Plant Dioecy, Ecology, Evolution and Sex Reversal

Brigham Young University BYU ScholarsArchive

Theses and Dissertations

1977-08-01

Plant dioecy, ecology, evolution and sex reversal

D. Carl Freeman Brigham Young University - Provo

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BYU ScholarsArchive Citation Freeman, D. Carl, "Plant dioecy, ecology, evolution and sex reversal" (1977). Theses and Dissertations. 8052. https://scholarsarchive.byu.edu/etd/8052

This Dissertation is brought to you for free and open access by BYU ScholarsArchive. It has been accepted for inclusion in Theses and Dissertations by an authorized administrator of BYU ScholarsArchive. For more information, please contact [email protected], [email protected]. C PLANTDIOECY: ECOLOGY,EVOLUTION

ANDSEX REVERSAL

I' /'>

A Dissertation

Presented to the

Department of Botany and Range Science

Brigham Young University

In Partial Fulfillment

of the Requirements for the Degree

Doctor of Philosophy

D. Carl Freeman

August 1977 This dissertation, by D. Carl Freeman is accepted in its present form by the Department of Botany and Range Science of

Brigham Young University as satisfying the dissertation requirements for the degree of Doctor of Philosophy.

ii ACKNOWLEDGMENTS

This study was performed under the guidance of Professor

K. T. Harper, who also provided partial financial support for the work. In addition to contributing many of the ideas embodied in this work, Professor Harper has also contributed his friendship for which I am most grateful. Drs. E. D. McArthur, Glen Moore, and

Eric Charnov have helped to mold the ideas presented, and Drs. K. T.

Harper, E. D. McArthur, Glen Moore and J. R. Murphy reviewed the manuscript and provided many helpful suggestions. Their efforts are gratefully acknowledged. Kent Ostler helped in compiling and analyzing portions of the data and his contribution is also gratefully acknowledged. My appreciation is also extended to my parents who have provided encouragement and support over many years.

Finally, my wife Loralee, has been most supportive and patient during the preparation of this thesis and I am grateful to her.

I thank Margaret Sharp for an excellent job of typing this dissertation.

iii TABLE OF CONTENTS

ACKNOWLEDGEMENTS• • • • • • • iii

AN ECOLOGICAL INVESTIGATION OF PLANT DIOECY IN WESTERi1 AMERICA . . . . . • • • ••.•.... 1

DIOECIOUS PLANTS AND THE ECOLOGICAL SIGNIFICANCE OF SEX REVERSAL ••••••••.••.•••.•..•..• 28

iv AN ECOLOGICAL HIVESTIGATION OF PLANT DIOECY

IN WESTERNAMERICA

1 INTRODUCTION

The typical sexual state of angiospermous plants is hermaphroditic, dioecious plants are considered to be botancial oddities.

Many authors have commented on nature's botanical experiment of creating separate sexed (dioecious) individuals. For instance,

Westergaard (1958) considered dioecy to be a failure. He reasoned that since this condition accounts for a low percentage of all seed plant species, the experiment has failed. There is ample evidence to substantiate the minor contribution of dioecy to the pool of seed plant species on earth. Yampolsky and Yampolsky (1922) reported that only 5% of the world's genera of higher plants are wholly dioecious. Lewis (1942) reported that only 2% of the species of the British flora are dioecious and Gilmartin (1968) fow1d 5% of the Hawaiian flora, 3% of the Ecuadorian flora and 3% of the Southern Californian flora to be dioecious.

Baker (1959) noted that dioecy is more co~mon among woody species than among herbs. Our findings tend to corroborate this conclusion since there is a strong positive relationship between woodiness and dioecy in the plant communities of the Intermountain

West. Several authors have noted that the tree floras of the tropics have a high percentage of dioecious species. For instance,

Bawa and Opler (1975) reported 22% of the tree species of Costa

Rica to be dioecious; 27% of the tree species of Hawaii are

2 3 dioecious (Carlquist 1966, Gilmartin 1968), and 26% of Malayan rain-forest trees are dioecious (Ashton 1969). The constancy of the values is surprising. However, it should not be concluded that the phenomenon of high percentages of dioecy among trees is unique to the tropics. The values reported above for entomophilous tropical tree floras are similar to those reported by Baker (1959) for trees in several plant communities of Britain. He found 25% dioecy among the tree species of the pedunculate oak forests, 20% in the sessile oak forests, 33% in beech woods, 29% in ash woods, and 20% among tree species of the pine woods. Unlike the tropical trees, however, many if not most of the temperate dioecious trees are anemophilous.

When all seed plants are considered, Westergaard (1958) appears to be correct in concluding that dioecy is a minor theme in the total seed plant flora of the earth. Although dioecy is relatively common among trees, herbs have a low incidence of dioecy and since they contribute so many more species to the world's

flora, the overall average of dioecy remains low.

In this paper, we will examine the ecology of the dioecious habit in plant communities of western United States. Dioecy will

be considered in relationship to the relative importance of anemoph-

ily in the vegetation, and the relative success of the woody habit

in the vegetation. The communities examined range from the deserts

of northwestern New Mexico to the alpine meadows and forests of the

Wasatch Mountains of Utah. All major communities in the region are

considered. We will also consider the distribution of dioecious 4 species mnong groups of species of similar lifcform or pollination behavior in the California flora.

METHODS

In all, we have assembled information concerning the compo- sition of 44 plant communities in the western United States. As shown in Table 1, the data have been drawn from the literature and the unpublished records of our own work and the work of colleagues.

The percentage of dioecy was tallied in two ways: 1) the percentage of dioecious species was determined for each community, and 2) the relative abundance of dioecious and hermaphroditic individuals was determined from quantitative samples of the community. Relative abundance was usually obtained from quadrat frequency values for prevalent species in a community. For a few communities (cold desert shrubs, shrub-grass, and blackbrush), frequency data were not available; in such cases, relative importance was computed from foliage cover data for prevalent species. The relative importance of anernophily, zoophily, shrubs, trees, or perennial and annual herbaceous species was also determined for each community from the quantitative data. Prevalent species were determined using the method of Curtis (1959). The number of prevalent species in a community is equal to the average number of species in a stand. If there are on the average 20 species per stand, there will be 20 prevalent species. Prevalent species are identified by ranking all species encountered in decreasing order of average quadrat frequency (or relative cover) in stands of occurrence. The prevalent 5 species arc selected from the top of the ranked frequency list in a number equal to the average number of species per stand.

In order to gain additional insight into the characteristics of dioecious plants, we have attempted to classify the 5000 plus

species of seed plants in the California flora (Munz 1968) with respect to sexual state (i.e., dioecious, monoecious, polygamous,

or perfect). Each species in the flora was also categorized in

respect to lifeform (annual, perennial herb, shrub, or tree) and

likely mode of pollination (wind or animal). A few (less than 20)

species of the California flora were omitted from analysis because

of the impossibility of accurately determining certain character-

istics. Many plants of the California flora, such as Clematis

ligusticifolia, show a variety of reproductive states. If a

species was listed as being monoecious or dioecious, we assumed a

conservative stance and tallied the plant as monoecious. Species

described as dioecious or polygamous were recoreded as polygamous.

Plants listed as polygamous or monoecious were treated as polyg-

amous. Presence or absence of a corolla, degree of exertion of

stamens, structure of the stigma, size of the flower, fusion of

floral parts, tendency of the corolla to restrict access to

nectaries, and corolla color were considered in making the

determination of most likely mode of pollination. Some errors

have undoubtedly been made in our categorization of reproductive

characteristics of various species, but the sample size is

sufficiently large that the analysis should not be seriously

impaired by occasional classification errors. 6 RESULTS

Dioecy in the Flora and Vegetation

Floristically, the communities range from Oto 20% dioecious

(Table 1). In terms of quantitatve measures of relative abundance of dioecious individuals, the communities range from 0-54% dioecious. The percentage of dioecy as determined by the two measures differs markedly: a Spearman rank correlation test (Steel and

Torrie 1960) showed no significant correlation between them.

Floristically, the values for percent dioecy are within the range reported earlier by Yampalsky &Yampolsky (1922), Lewis (1942), Gilmartin (1968), Baker (1959), and Ashton (1969). The values for percent dioecy based upon quantitative measures (Table 1) are the only known values for temperate communities.

Dioecy and Anemophily

We have correlated percent dioecy with percent anemophily in the 44 communities. On a floristic basis, a significant positive relationship exists (r = .349, p < .05). A stronger positive relationship is found when the relative success of dioecious individuals in a community is regressed on the relative abundance of anemophilous individuals in the same community (r = .40, p < .01).

This is the only portion of our data analyses where both floristic and vegetation measures of dioecy yield closely comparable results for correlation analyses. The floristic measure of percent 7 dioecy was not significantly correlated with floristic measures of woodiness of the vegetation or with diversity of the flora.

Accordingly, we will use only quantitative measures of the relative success of a characteristic in the regression analyses reported hereafter.

A Chi-square analysis of the California flora data (Table 2) shows that anemophily is overrepresented in dioecious as opposed to perfect (both sexes in the same flower) flowered species 2 (x = 745, p < .001). Grant (1951) and Baker (1959) have reported a similar relationship between dioecy and wind pollination.

Dioecy and Woodiness

The relative importance of the dioecious habit is positively correlated with the relative success of woody species in the communities considered in our study (r::,: .440, p < .01). Likewise, in the California flora, dioecy is better represented among woody 2 species than among herbs (x = 387, p < .01; Table 3). Baker

(1959) and Stebbins (1951) also concluded that dioecy is primarily a phenomenon of woody plants.

Several authors (Baker 1959, Grant 1951, Stebbins 1951) have noted that anemophily and woodiness are strongly correlated with dioecy in the temperate zones of the earth and are also positively correlated with each other. We also find that woodiness and anemophily are positively correlated in the plant communities considered in this paper (r = .606, p < .01). Chi-square analysis of the occurrence of anemophilous and zoophilous species among the 8 various lifeform groups in the California flora (Table 4) shows that anemophily is greatly overrepresented among woody species 2 there too (x = 355, p < .01).

Since both woodiness and anemophily are positively correlated with the dioecious habit among seed plants, it would be helpful to know whether both characteristics predispose plants to dioecy or where only one (or neither) exerts a causal influence.

This question cannot of course, be tested directly, but one can test for statistical interactions between those variables as they relate to the success of dioecy in a suite of communities. We have experimented with the use of the interaction of woodiness and anemophily (i.e., % woodiness of a vegetation was multiplied by % anemophily in the vegetation) in a simple regression analysis in which relative success of the dioecious habit is the dependent variable. The 44 plant communities again provided the data base.

The results yield a correlation coefficient of .61 (p < .01).

Since the simple correlation coefficients for% woodiness versus% dioecy and% anemophily versus% dioecy (.440 and .349 respectively) are much smaller than the r-value obtained use the interaction of woodiness and anemophily, we infer that both woodiness and anemoph-

ily may be acting in concert to predispose species toward the dioecious habit.

DISCUSSION

The dioecious habit predictably occurs with greater

frequency in certain types of environments. As supported herein 9 and reported elsewhere, dioecy occurs primarily among anemophilous, woody plants. The condition appears to have evolved independently in numerous plant families. In fact, Westergaard (1958) reported that dioecy occurs in 75% of the families of higher plants. It would seem logical to assume that strong selective forces are responsible for the massive convergence of many diverse genetic stocks onto the dioecious habit. What are those forces?

We believe that part of the answer to why dioecy is so prevelant in the semiarid Intermountain West lies in the fact that a large percentage of the flora there is pollinated by wind.

Anemophily succeeds there because the flora is impoverished and many species have the capacity to produce large local populations.

These characteristics provide assurance that pollination by wind can be successful. Since wind pollination may be less expensive energetically than zoophily (petals, odors, and nectar can be abandoned), it seems possible that anemophily has displaced zoophily wherever the former process can produce adequate reproduction.

It seems probable that most dioecious plants in semiarid regions of western United States are derived from wind-pollinated ancestors. In this region, heavy concentration of dioecious species in such prevailingly anemophilous families as Chenopodiaceae,

Ephedraceae, Poaceae, and Salicaceae provide some of the evidence for this conclusion. In an environment in which available soil moisture varies strongly among local microsites, disruptive selection would tend to differentially affect the success of male and female gametes of anemophilous species on common sites. Thus, male gametes from plants of ridges and steep slopes may not be seriously 10 disadvantaged by dry growing seasons. However, the female function of plants on such sites would largely fail in dry years, since heavy metabolic demands would be made on the plant producing seed long after soils dried. Plants in depressions where soils are deeper and more fully recharged by runoff water would more consis- tently produce good seed crops. Pollen production in these latter sites may be no greater than for plants on ridges, however, since pollen is shed early in the season while all soils are usually ' moist from the winter storms which contribute most of the biologi- cally usable moisture in the region. Furthermore, pollen produced on depressional sites may actually be dispersed less well than pollen from individuals on ridges, because of a more dense cover of nonreceptive plant surfaces on the depressional sites and reduced wind movement (Freeman et~- 1976).

Fortuitously, disruptive selection as outlined above would tend to maximize the reproductive efficiency of populations diverging toward the dioecious habit. Such disruptive selective forces would tend to favor separation of the sex organs onto different individuals. Individuals tolerant of ridgetop conditons would regularly contribute large inputs of male gametes to the species; individuals best fit for moist depressions would contribute more female gametes than individuals on ridges. Any genetic rearrangements that linked maleness to fitness for ridgetops or more xeric sites and femaleness to adaptations for optimal performance on more favoT,ble sites would be selected for. Competition of both an intra- and interspecific nature would reinforce the disruptive selection. 11

It is instructive to examine selected communities in respect to dioecy and the potential for water stress, since water stress could conceiveably exert a disruptive force on perfect flowered genotypes and derive from the species the dioecious condition. The limber pine community shows a much higher percentage of dioecy than any of the other coniferous forest types. This community is confined to high elevation ridges with shallow soils and great exposure to wind. Consequently, large amounts of snow (the major source of usable water for plants in this region) would not accumulate in the community and the shallow soils would further reduce the supply of moisture avaiable to plants during dry periods. Wind would acceler- ate water loss and thus intensify water stress. Other coniferous forest types of the mountains appear to be much less stressed for water. In the same vein, shadscale communities border sagebrush communities but occupy a more xeric environment: the percentage of dioecy is much higher in the shadscale community. Thus, there appears to be a correlation between water stress and the dioecious habit among upland communities, but dioecy is also a common theme in gallery forests along streams (Table 1 and Bawa and Opler 1977).

However, Freeman ~t al. (1976) have noted that even along streams at least one dioecious species segregates along the moisture gradient encountered as one moves away from free flowing water. 12

Evolution of the Dioecious Habit

Historic Arguments

Dioecy has long been held to have evolved as a means to promote outcrossing (Baker 1959, Bawa &Opler 1975, Darwin 1889,

Gilmartin 1968, Grant 1951, Lewis 1942, Mather 1940, Stebbins 1974,

Stebbins 1951, Weins & Barlow 1975, Westerga~ l 1958). Such arguments are exemplified by Mather (1940) who argued that, "There is, however, one inevitable consequence of the dioecious state which enables us to understand its occurrence. If the sexes are separated, fertilization must always involve gametes from different zygotes and, in the vast majority of cases, these zygotes must be genetically distinct. It is essentially a mechanism for the promotion of outbreeding. An increase in the effective recombi- nation allows a more rapid response to the action of natural selection." Bawa and 0pler (1975) state the argument more concisely: "We feel the main selective advantage of the dioecious habit is due to its enforcement of outcrossing." Thus, it has been argued that because dioecy promotes greater outcrossing, it has been favored.

An Alternative Argument

We do not wish to minimize the adaptive advantage of outcrossing as a consequence of the dioecious habit, but we do believe that excessive reliance on the outcrossing argument has been detrimental to a balanced view of the evolution and consequences of 13 the dioecious habit. There is, for example, a tendency to ignore or minimize the penalties a species incurs when it becomes dioecious

(Bawa and Opler 1975). Seed set in the newly evolved dioecious population will be reduced by at least half assuming a 1:1 sex ratio and unchanged seed set per seed producing individual.

Furthermore, if we assume that sex is irrevocably fixed, there must be heavy seedling mortality losses in semiarid and arid environments where males have been shown to be overrepresented in harsher microenvironment and females in more favorable microenvironments

(Lysova and Khizhnyak 1975, Richards 1975, and Freeman et~- 1976).

Inbreeding depression as the sole driving force behind the evolution of the dioecious habit also fails to account for some conspicuous correlations between dioecy and various plant characteristics. For example, why have entomophilous species as a group tended to circumvent inbreeding by evolving mechanisms for self-incompatibility while anemophilous species have prevailingly employed dioecy? A. priori, it would appear that a self-compatible, entomophilous plant would be more highly selfed than a self-compatible anemophilous plant. While the nectar reward provides insects with an incentive to visit blossom-after-blossom on the same individual, the wind cannot be conditioned to confine its pollination activities to a single individual. Since wind- pollinated plants often bloom before the leaves are out, turbulence should be minimal and pollen movement should be fairly unidirec- tional. Pollen on the periphery of leesides of plants will be moved to adjacent individuals. This is not true with the insect which may visit blossom-after-blossom of the same individual, thus 14 moving pollen from even peripheral locations to stigmas of the same individual. If we conservatively assume that wind and insects cause the same amount of selfing in self-compatible species, there should exist 124 dioecious zoophilous species and 21 wind pollinated dioecous species in the California flora (Table 2). In reality, only 10 dioecious species are animal pollinated while 135 dioecious species are pollinated by wind. Thus, there are 13.5 times as many wind as animal pollinated dioecious species. Yet, there are over five times as many zoophilous species. It is unlikely that wind causes over 65 times as much selfing as animal pollinators.

Segregation of the sexes of dioecious species in space is another pattern which cannot be accounted for by the postulate that inbreeding depression is the primary force behind the evolution of the dioecious habit. Spatial segregation of the sexes of dioecious species has been reported by Gregg (1973), Lysova & Khizhnyak

(1975), Richard (1975) and Freeman et~- (1976). If inbreeding depression were the sole factor in the evolution of the dioecious habit, there would be no reason for the sexes to be differentially distributed in space. Some may argue that the segregation of the sexes evolved after the dioecious habit arose, but it has been shown that male flowers of several monoecious species are proportionately more abundant than female flowers on dry sites while the reverse is true on mesic sites (Barker et al. in review and Freeman et al. in review). Thus disruptive selection was acting to spatially separate the male and female reproductive functions before the evolution of the dioecious habit. 15

We propose the following evolutionary scheme which accom- modates the patterns mentioned aboYe (i.e., the correlation between anemophily and dioecy and spatial segregation of the sexes), and explains why most dioecious species are woody. As we have noted earlier, anemophily appears to antedate most cases of dioecy in the arid regions considered here. We have also outlined how disruptive selection tends to favor maleness on dry sites and femaleness in more moist microsites. Ultimately such selection appears capable of generating male and female individuals. It seems reasonable to assume that male and female individuals have been spatially segre- gated from the inception of the dioecious habit. If the heterozygotes prove more fit than the homozygotes, inbreeding depression should allow for gonochore genes (genes for separate sexed individuals) to spread. If homozygotes prove more fit, inbreeding would reinforce the concave fitness set established by disruptive selection and still facilitate the spread of gonochore genes (Levin 1967). Anemophily appears to maximize the various processes (e.g., separation of sexes in the inflorescence, inter- individual pollen flow, and optimal male performance in harsh, convex sites) that favor disruptive selection and give rise to dioecious individuals. The entire process is facilitated by inbreeding.

Woodiness becomes involved in most cases of dioecy because size of individual appears to have a profound influence on the incidence of inbreeding. Logic suggests that self-compatible, anemophilous woody plants will be more highly inbred than will self-compatible, anemophilous herbs. This should be true simply 16 because of the relative size of herbs and ,voody plants. Wind passing through a tree or shrub canopy will move available pollen across numerous stigmas of the same individual. In contrast, pollen from small herbs would be expected to encounter few stigmas of the same individual.

We thus conclude that anemophily operating in a habitat that is strongly heterogenous for water, a critical resource, tends to maximize the disruptive forces which select for gonochore genes: spread of those genes is facilitated by inbreeding, an inevitable consequence of woodiness and large plant size. The data of Baker

(1959) support this conclusion. He stated, "of the 97 families know to contain self incompatible or dioecious species, only 13 contain both. These are almost all very large families. Even when they occur in the same family it is usual for the two kinds of outbreeding systems to be found in separate genera." Thus, many dioecious species appear to have arisen from self-compatible ancestors. One would expect that large, hermaphroditic, self- compatible plants would have a high degree of both self-fertilization and familial matings. Wind as opposed to animal pollination could be expected to reduce inbreeding in such species. Anemophily would also enhance the efficiency of disruptive selective forces which optimize gamete production in strongly heterogenous environments.

The disruptive selective forces would also reduce the amount of inbreeding depression necessary for the spread of the gonochore genes.

Further, upon examination of the communities which exhibit a high percentage of dioecy on a quantitative basis we see that the 17 riparian and cold desert shrub communities are among the highest.

It would be reasonable to assume in both cases that many of the matings would be familial matings, thus increasing the inbreeding and allowing for a rapid spread of the gene. Both communities also exhibit great environmental heterogeniety so disruptive forces should play a significant role in generating separate sexed individuals.

CONCLUSION

We have shown that the dioecious habit is not equally represented among the plant communities of western North America.

In some communities, over 40% of the individuals encountered many be dioecious. Dioecy is best developed in plant communities that also emphasize anemophily and woodiness. We also show that dioecy is not randomly distributed among the lifeform groups of the flora of California: dioecy is predominately a breeding strategy of woody plants. It is also a breeding strategy that is overrepresented among anemophilous plants in western NoTth America. We believe that the dioecious habit has arisen repeatedly through disruptive selection processes that are maximally effective in patchy environments dominated by anemophilous, woody species.

Dioecy in the region considered appears to arise as a consequence of unequal success of male and female gametes on common sites in a patchy environment. Inbreeding depression facilitates spread of genes that impart dioecy but is probably not the major force selecting for those genes as others have postulated. BIBLIOGRAPHY

Ashton, P. S. 1969. Speciation among tropical forest trees: some deductions in light of recent evidence. Biol. J. Linnaen Soc. London 1:155-196.

Baker, H. G. 1959. Reproduction methods as factors in speciation in flowering plants. Cold Spring Harbor Symp. Quart. Biol. 24:177-191.

Barker, P., D. Carl Freeman and K. T. Harper. In review. Sex reversal in Acer grandedentatum.

Bawa, K. S. and P.A. Opler. 1975. Dioecism in tropical forest trees. Evol. 29:167-179.

Carlquist, S. 1966. The biota of long distance disperal IV Genetic Systems in floras of oceanic islands. Evol. 20:433-455.

Curtis, John T. 1959. The vegetation of Wisconsin. University of Wisconsin Press, Madison.

Darwin, C. 1889. Different forms of flowers on plants of flowers on plants of the same species D. Appleton and Co., New York.

Freeman, D. C., L. G. Klikoff and K. T. Harper. 1976. Differential resource utilization by the sexes of dioecious plants. Science 193:597-599.

Freeman, D. Carl, E. D. McArthur and K. T. Harper. In manuscript. Differential resource utilization of male and female flowers of monoceious species.

Gilmartin, A. J. 1968. Barker's law and dioecism in the Hawaiian flora: An apparent contradiction. Pac. Sci. 22:286-291.

Grant, V. 1951. The fertilization of flowers. Sci. Amer. 184:52-56.

Hall, H. H. 1971. Subalpine Meadow Ecology. Thesis, University of Utah.

Harper, K. T. 1976. Permanent plot native vegetation studies. pages 20:436 in A. C. Hill, et al. Vegetation air pollution investigations in the vicinity of the four corners and San Juan Power Plants .. Environmental Studies Laboratory, University of Utah Research Institute, Salt Lake City 350 p.

18 19

Jaynes, R. and K. T. Harper. The relative responses of selected plant lifeforms to environment in southwest United States. (manuscript in preparation).

Kleiner, E. F. and K. T. Harper. 1972. Environment and community organization in grasslands of Canyonlands National Park. Ecology 53:299-309.

Levin, R. 1967. Evolution in changing environments. Princeton Univ. Press. Princeton, New Jersey.

Lewis, D. 1942. The evolution of sex in flowering plants. Biol. Revs. Cambridge Phil Soc. 17:46-67.

Lysova, N. V., and N. I. Khizhnyak. 1975. Sex differences in trees in the dry steppe. The Soviet J. of Ecol. 6(c)522-527.

Mather, K. 1940. Outbreeding and separation of the sexes. Nature 145:484-486.

Munz, P. A. 1968. A California flora. University of California Press.

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Steel, R. G. D. and S. H. Torrie. 1960. Principles and procedures of Statistics. McGraw-Hill Book Co., New York, Toronto, London.

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Table 1. The relative importance of dioecy, plant woodiness, and anemophily in fourty-four plant communities of western United States. Importance of each characteristic in each community is computed two ways: 1) percent of prevalent species showing trait, and 2) percent of the sum of frequency of all prevalent species contributed by species possessing the trait. Number of stands averaged in each community and source of information is also shown.

Table 2. Chi-square analysis of dioecious and perfect flowers among zoophilous anemophilous species. It is apparent that dioecious species are prevailing anemophilous (P < .01).

Table 3. Chi-square analysis of the distribution of zoophily and anemophily among the lifeform groups. The summation chi-square value obtained departs significantly (P < .01) from random expectation.

Table 4. The distribution of dJoecious and perfect flowered species among the lifeform groups. The departure from random expectations is significant (P < .01). TABLE1

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,.; .., .c 2 •I; r_.:; vi ,,., s c' ·,: :! ·;.: co,, ,, r.. .,1 .., :..4-..---t >- ,: ; ~. :, n ..1.--: riJ d •r, :~,t ~= () '/) ,--1 :; '",. ·:::•·;•-· (J ;-• i, 'J) () c:: ·,--1 :;J ,-; •') µ n ·n ;:j ~' :-' ') :~ t > ' I -., _JS-, -Tj :..1 "-· -: u; n. p " _,. 1_1 <"I !...; '·•". (1 0 • " -'._) ,J..: ...-,: < u ,_J ? ) - f,/j 24

,_, .... C,"'

.cf~ r----l"' Vl ::, M .,.... C, u ,-.. l;) --i $,, CJ - -:-.l 0.. f.l .p U) 0 ,., r o

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c'? ,,--_ -~"' >-. µ V,:; c,, 0 µ "' () ·d ,,, .- p ,,, ""M 6

0 >,•M n-; ,,, 0, ;~-~ N 0 <' - ~=_:,

Cl ,O

0 '.;--,•d 0 .;...> 0 •:1

•d0 "'H 0 CO C • --< .,;/~ t") t') ~- ,..:; 6t-.... ,r ... .µ~pc;. :1 ,,--, ff') H -, "J ,,., 'll ,-1 2, u ,-.._ (.) (J ,_ ,___., '------"' ;" 8'~j~ S:.L-8 . ~g . 1 I :=, ;.~ :r:~,,} ·;1 ~1

,c:,, ,,.1 ,..'/..n •J M r< "1 25

TABLE2

Anemophily Zoophily

Dioecious 135 10

(21. 03) (123.97)

Perfect 559 4082

(672.97) (3968.03) 2 x = 745 26

TABLE 3

Herbaceous Annual Tree Shrub Perennial Herb

Dioecious 18 87 48 2

(3.24) (18. 82) (83.39) (49.55)

Perfect 82 494 2527 1528

(96. 76) (562.18) (2491.61) (1480. 45) 2 x = 387.44 27

TABLE4

Herbaceous Tree Shrub Perennial Annual

Zoophily 26 509 2433 1483

(102.17) (520.59) (2460.25) (1367. 98)

Anemophily 100 133 601 204

(23.83) (121.41) (573.75) (319.02) 2 x :: 354.36 DIOECIOUSPLANTS AND THE ECOLOGICAL

SIGNIFICANCEOF SEX REVERSAL

28 Current literature assumes that sex in dioecious plant species is constant and determined chromosomally (Lloyd 1974a, 1974b, 1975; Mulcahy Rysclewski & Kaximierz 1975; and Weins and

Barlow 1975). Nevertheless the results of the researchers who discovered how sex is inherited in plants demonstrate that "males" have the potential of developing carpels (Yampolsky 1919, Sansorne 1938, Kuhn 1939, Rick &Hanna 1943, Heslop-Harrison 1964) and setting seed while "females" may produce stamens with viable pollen (Heslop-Harrsion 1924, 1957, 1963, 1966, 1972). In addition, many dioecious plants are known to produce hermaphroditic offspring

(Correns 1928, Love 1945, Allen 1942).

The idea that sex in dioecious species is constant and chromosomally determined has persisted despite the existence of a large literature that demonstrates the inconstancy of sexual expression in dioecious species and the complexity of its inheritance.

The current, simplistic position still maintained by many is perhaps explained by the fact that early workers were trying to establish the existence of sex chromosomes in plants: it was only natural that they did not dwell on the existence of hermaphrodites in prevailingly dioecious species. Nevertheless, those workers realized that hermaphrodites are normally found in dioecious plants species and that reversal of the sexual state of individuals did occur

(Correns 1928, Yampolsky 1919, Hirata 1924, Allen 1942, Love 1945).

Indeed, Hartmann (1956) has formulated "The law of the bisexual 29 30 potentiality of both sexes" a view supported by Yampolsky (1919),

Correns (1928), Allen (1940), Westergaard (1958), Heslop-Harrison

(1924, 1957, 1964, 1972), Gregg (1973) and Janzen (1977). Early workers also established the importances of autosomes in determining sex. It has been shown that in some species, at least nine pairs of chromosomes are involved in sexual expression (Allen 1940).

Recent investigators of unbalanced sex ratios among plants generally assume that sex is determined by sex chromosomes (whether or not the chromosomes are heteromorphic) and that dioecy has been selected for because it provides for escape from inbreeding depression (Connors 1973, Lloyd 1974a, 1974b 1975c; Lysova and Khizhnyak

1975, Richards 1975, Rychlewsk and Kaximierz 1975, Bawa and Opler

1975). In combination, these assumptions would seem to argue that the sexual state of an individual is irrevocably determined by genetics. Recent work by McArthur (1977) demonstrates, however, that environmental stress can induce individuals of at least one species (Atriplex canescens) to switch sex.

To illustrate how readily sexual expression in flowering plants can be altered, we have listed in Table 1 factors known to promote sex reversals in higher plants and the direction of change.

In addition, the literature demonstrates that many dioecious plant

species exhibit sex reversal or give rise to hermaphroditic offspring

(Table 2). It should be noted that many of the species that have been observed to switch sex have sex chromosomes (Table 2). Since researchers rarely examine the same individual year-after-year, we

are unable to determine whether the observed hermaphrodites persisted 31 throughout their life in that state or whether they occasionally reverted to a unisexual state.

The labile nature of sexual expression among many dioecious plant species is apparent from Table 2. Twenty-six families and over SO species are represented. Of those species, 16 have been reported to have sex chromosomes. Indeed, of the 13 species

Westergaard (1958) lists as having well established cases of heteromorphic sex chromosomes, eight are known to·exhibit either sex reversal or to produce hermaphroditic offspring. Of the 39 species which Westergaard lists as being "questionable or insuffi- ciently established cases of heteromorphic sex chromosomes in plants", eight appear on our list, and four others have congeners which exhibit sex reversal or produce hermaphroditic offspring.

The literature abundantly testifies that determination of the sexual state is genetically complex even in species with distinct sex chromosomes. Futhermore, sexual expression in some species is known to be subject to some environmental control (Schaffner 1918,

1919, 1921, 1922, 1923a, 1923b, 1923c, 1925a, 1925b, 1925c, 1926,

1927, 1928, 1930, 1931, 1933, 1935, Heslop-Harrison, 1924, 1957,

1964, Minnia 1952, Dzhaparidize 1963, Gregg 1973, Richards 1975,

1957, 1961, 1972, McArthur 1977).

Our purpose here is not to reiterate how sex is determined, since that has been done masterfully by Correns (1928) Allen (1940), and Westergaard (1958). Nor is it necessary here to elucidate the myriad of ways by which the physiologist has altered the sexual expression of individuals: Heslop-Harrison (1957, 1964, 1972)

Dzhaparidize (1963) and Gregg (1973) have provided excellent reviews 32 of that literature and added their own insightful observations.

What we propose to offer is an ecological explanation for the phenomenon of sex reversal and a hypothesis concerning the conditions under which reversal should occur. We will also suggest new avenues of research.

Ghilsen (1969) has suggested "where an individual reproduces most efficiently as a member of one sex when small or young, but as a member of the other sex when it gets older or larger, it predicts proterogyny where there is sexual selection for larger males, and protandry where the younger stages must hunt for a suitable environment." This theory has been applied to reef fish and greatly expanded by Warner et ~-, (1975), Leigh et ~- (1976) and Charnov and Bull (1977). Warner et ~- (1975) have noted in their studies of the blue headed wrasse that individuals changed from female to male when they could defend a breeding territory. While the equations used by Warner et al. (1975) and Leigh et al. (1976) dealt with the age of the individuals, this was done for convenience. The salient parameter was size: the individual changed sex when it could defend a given resource, a territory.

We believe with Janzen (1977) that a somewhat analogous condition exists in dioecious plants. It is known that individuals of Arisaema draconteum or~- triphyllum (Shaffner 1925), Arisaema japonicus (Maekawa 1929), and Eucommia ulmoides and Castilloa elastica (Dahaparidize 1963) normally produce male flowers first.

It is only after several seasons that the individuals produce female flowers. The percentage of female flowers apparently increases with age. It has also been demonstrated that sex and 33 pseudocorm size are related in several species of orchid (Gregg

1973). This is also suggestive of sequential hermaphroditism, especially since these species are known to exhibit sex reversal

(Gregg 1973). We (Harper and Freeman unpublished data) have observed a similar correlation between size and sex in Atriplex confertifolia with the smaller individuals being male. In addition McArthur and

Freeman (unpublished data) have shown that males of A. canescens have a smaller crown diameter than females. The latter example is especially suggestive of sequential hermaphroditism, since A. canescens is known to change sex under stress (McArthur 1977).

There are, of course, differences between the sequential hermaphroditism exhibited by the blue headed wrasse and that suspected for dioecious plants. When the fish reaches a given size, it becomes male for life and defends a breeding territory that is apparently a relatively stable resource. In contrast, the resource important to plants may fluctuate strongly and frequently. This is particularly true for water in arid and semiarid environments. If sexual expression in plants is correlated with a resource state, it would be advantageous for plant sexual expression to fluctuate in synchrony with variable environments.

Schaffner (1922, 1925a, 1926) and others listed below have

shown that the sexual expression exhibited by an individual is

indeed related to its physiological state. He found that if he

removed a portion of the corm from a female of Arisaema dracontium

or!::_. triphyllum, the plant would exhibit one of three sexual states

when it flowered again depending upon the amount of corm removed.

If he removed a relatively small amount, the plant became monoecious. 34

Removal of a slightly greater amount produced male plants, and removal of a greater amount still resulted in nonflowering. As a plant recovered, it would pass through the stages in reverse order,

(i.e., if a sufficient amount of the corm was removed to cause a female to change sex and become male, in the course of recovery the plant would first produce male, then monoecious, and finally female flowers.

Other cases are known in which stressed plants revert to the male state. McArthur (1977) found that in the flowering season following an unusually severe winter, 86 females of Artriplex canescens became either male or monoecious, 10 monoecious individuals became male, but only eleven male and monoecious individuals became female. Obviously, the stress triggered a shift towards maleness.

The following years were relatively normal and there was a shift back towards femaleness in McArthur's (1977) population. Cold in the form of frost damage has also been reported to trigger a similar shift from femaleness to maleness in cycads (Menniger 1967).

Minina (1952) has shown that under conditions of either low soil moisture or low relative humidity, cucumbers have only male flowers. The female sex organs in wheat are likewise more suscep- tible to water stress than are the male organs (Minina 1952).

Lysova and Khizhnyak (1975), Richards (1975) and Freeman -- et al. (1976) have all shown that in a variety of dioecious plant species males are proportionately more abundant than female in xeric habitats and that females out-number males in more mesic environments.

Schaffner (1925a) has shown that well fertilized plants tend to be female; he and others (Giard 1898, Davey and Gibson 1917, 35

Mukerji 1936, Dzhaparidize 1963, Brubaker 1969, Gregg 1973) have concluded that the burden of seed production is commonly borne by the most vigorous individuals.

Data also exist that suggest that environmental variables other than that available moisture, nutrients and storage reserves can induce sex reversal. Gregg (1973) has shown that sex reversal is related to light intensity in several monoecious to dioecious orchid species. Plants in the shade are usually male, but when such plants are placed in the sun they become monoecious or female.

Likewise, females may become monoecious or male when placed in the shade. In nature, males are normally most abundant in the shade, while females are more prevalent in the sun. Thus, the orchids show differential resource utilization between the sexes but unlike dioecious species of temperate or semiarid to arid habitats, they segregate along a gradient of light intensity.

It is interesting to note that Bawa and Opler (1977) have found no segregation of the sexes of tropical trees in Costa Rica along a gradient of available soil moisture. Gregg's (1973) work suggests that if the sexes do segregate there, they are most likely to do so along the light gradient which should be strong in tropical forest. An examination of the sex ratio of dioecious trees in the upper canopy and in subdominat positions in the lower canopy (or on the edge of gaps created by fallen trees and in adjacent, undisturbed forest) would provide a series of quick and useful tests of the basic theory proposed above.

Although most references that we have consulted treat sex reversal as an unusual event of intellectual interest but of no 36 ecological consequence, McArthur's (1977) data suggest that the phenomenon may be common and of considerable consequence ecologically. He found that 25% of individuals in a seed orchard of A. canescens changed sex in a stressful year. This is the only report we are aware that notes the extent of sex reversal under field conditions.

It seems likely that sex reversal has not received serious consideration by field workers simply because they have not seen an adaptive advantage to individuals which change sex. Nevertheless, the data suggest that for dioecious species which exhibit spatial segregation of the sexes, individuals producing offspring capable of changing sex in response to environmental stimuli will always have a selective advantage over individuals of invariate sex. Four research groups, widely separated geographically and dealing with such diverse taxa as Aceraceae and Oleaceae (Lysova and Khizhnyak 1975), Rosaceae

(Richards 1975), Orchidaceae (Gregg 1973), Aceraceae, Ephedraceae,

Chenopodiaceae, Poaceae, and Ranunculaceae (Freeman et al. 1976) have independently shown that the dioecious species investigated exhibit a spatial separation of the sexes. All of those workers reported similar distribution of males and females in space (i.e., males are most often encountered in harsh environments while females are found most often on favorable sites). It is also known that in monoecious (Freeman et~- 1977a) and polygamous (Barker et al.

1977) flowered species, male flower are proportionately more abundant on xeric sites while female flowers out-number males on mesic sites.

It thus seems likely that the tendency for plant sexes to segregate 37 along strong resource gradient is not confined to dioecious stock and may have arisen before dioecy itself (Freeman et ~l- 1977a). Differential distribution of plant sexes in space could arise in at least three ways: 1) the pattern may arise from differential dispersal of seeds of opposite sex, 2) seedling of opposite sex may show differential survival on sites of differing quality, and 3) sex could be labile. There is no evidence in the literature to suggest differential dispersal of seed. Furthermore, the seeds of many of dioecious species we have studied are dispersed by wind

(Freeman et~- 1976). The seeds of such species would be expected to travel up to several score meters away from the parent plant, yet the sexes of these species often show spatial segregation ¼ithin 10 meters or less. Such data suggest that differential dispersal is not important, nevertheless conclusive research is lacking.

Lysova and Khizhnyak (1975) suggest that the observed segregation of the sexes in their study may have resulted from differential mortality of different sexed individual~ on sites of unequal quality. However, they based their opinion on the distribution of adults only. They did not explore the mechanism of segregation.

Assuming that the observed differential distribution of males and females in space is ecologically useful and has been selected for, it would appear to be counter productive to achieve this condition through differential seedling survival. When a gene producing separate sexed individuals first appeared in a hermaphroditic population, it could spread only if 2N F < N F where N is 1 1 2 2 1 the average number of seed produced by the hermaphrodites, F is 1 38 the average fitness of those hermaphrodites, N is the average 2 number of seed produced by dioecious individuals and F is the 2 average fitness of those offspring. We have assumed a 1:1 sex ratio. If we further assume random dispersal of male and female seeds, and that a male environment is lethal for a female and vice versa, then in order for the gene producing dioecious individuals to spread, the following relationships must hold: 4N F < N F . This 1 1 2 2 relationship would exist since 1/2 of the seed could be expected to land in an environment favoring the opposite sex and thus be wasted.

These are very rigorous conditions. Individuals which produce seeds capable of switching sex would only have to meet the conditions of the first equation. As a consequence, in dioecious species which exhibit spatial segregation of the sexes, individuals which produce offspring with the capacity to change sex should always be at a selective advantage.

It is relatively easy to understand why a female inhabiting a site of changing quality may in unfavorable years become monoecious or male. As we (Freeman et~- 1976) have elsewhere argued, there are usually greater energetic and resource costs associated with being female as opposed to male. Lysova and Khizhnyak (1975) have shown for Acer negundo and Fraxinus lanceolata that males and females on similar sites grow at equal rates until the females mature the first seed crop. After the onset of seed production, females appeared to grow at a slower rate than males. The difference between the growth rates of males and females was believed to increase with the number of seed crops produced by the female. Stark (1970) has shown that on common sites, females of Atriplex hymenlytra were 39 under greater water stress than are males. It seems possible that females that became male under such stressful conditions may survive better than females incapable of changing sex.

We have elsewhere shown that the dioecious habit is not randomly distributed among lifeform or pollination groups or plant communities (Freeman et al. 1977b). Most dioecious species are woody, wind pollinated and inhabit relatively harsh environments.

Dioecious plants reach maximal importance in the vegetations of arid environments in the western United States. In such environments, the bulk of the effective precipitation occurs in the winter months, and pollen is shed in the spring under favorable moisture conditions.

Females, however, must bear the burden of seed production throughout the long, dry summer. Plants capable of deemphasizing femaleness or becoming male in unusually dry years almost certainly would be at a competitive advantage in such environments.

One might logically expect that females that became males would be selected for in the arid environments of western United

States. Such individuals could transmit genes to the next generation through females occupying more favorable sites without seriously endangering their own chances of survival into another and perhaps more favorable year. There thus appears to be a rational explanation for females that change sex. But, why do males become female, especially since females are more stressed than males? Assume a male normally fertilizes X ovules, and produces Y pollen grains at a resource cost Z. If pollen is plentiful and a male must produce

X + ~X pollen grains in order to fertilize X + 1 ovules at a cost of z +~Zand z + ~Z is greater than the cost of changing sex and 40 producing Y + I ovules, then selection will favor the male that switches sex under optimal conditions.

Pollen production is large in most wind pollintated species and Freeman et al. (1977b) have shown that the majority of temperate dioecious species are wind pollinated. Further we (Freeman et~-

1976) have shown that most males are found on ridges exposed to wind and thus in a position for effective pollen dispersal. However, we have not determined the male's cost of fertilizing one additional ovule as opposed to the female producing one more seed. We offer the foregoing explanation as a hypothesis and await the results of experiments which are in progress. If the hypothesis is valid, the theory we have outlined is equivalent to that proposed by Ghilsen

(1969), Warner et al. (1975), Leigh et al. (1976), and Charnov and

Bull (1977).

CONCLUSION

We have shown that sex is labile in many dioecious species.

Furthermore, many plants reported to have sex chromosomes have the potential of producing monoecious offspring and/or reversing sex.

We have also shown that dioecious individuals of patchy or changing environments which have the capability of sex reversal will have a

selective advantage over individuals lacking this ability. In addition, we have postulated reasons why individuals of each sex

should have the potential of developing flowers of the other. Sex

switching permits dioecious species to optimally exploit the resources of environments that are heterogeneous in time and/or

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Kuhn, E., 1939. Selbstbestaubungen subdiocischer blutenpflanzen, ein neuer beweis fur die genetische theorie der geschlechtsbestimmung. Planta 30:457-470.

Leigh, Egbert G., Jr. Eric L. Charnov, and Robert R. Warner. 1976. Sex ratio, sex change, and natural selection. Proc. Natl. Acad. Sci. 73:10:3656-3660.

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Lilienfeld F. A. 1936a. Karyologische und genetische studien an Fragaria III. Geschlechtsverhaltnisse in den F - und 2 weiteren folgegeneratjonen des bastards aqischen der getrenntgeschlechtigen F. elatior und der zwittrigen !:_. nipponica. Mem. Coll. Agr. Kyoto lmp. Univ. 38:1-58.

Lilienfeld, F. A. 1936b. Karyologische und genetische studien an Fragaria II. 1st Fragaria elatior eine autopolyploide Pflanze? Jap. Jour. Bot. 8:119-149.

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Negi, S. S. and H. P. Olmo. 1966. Sex modification in grapes by cytokinin. Sci. 152:1624-1625.

Negodi, G. 1929. Ricerche sulla distribuzione e transmissione

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Schaffner, J. H. 1921. Influence of environment on sexual expression in hemp. Bot. Gaz. 71:197. 47

Schaffner, J. H. 1922. Control of sexual state in Arisaema triphyllum and A_. dracontium. Am. J. Bot. 9:72.

Schaffner, J. H. 1923a. TI1e influence of relative length of daylight on the reversal of sex in hemp. Ecol. 4: 323.

Schaffner, J. H. 1923b. Sex reversal in the Japanese hop. Bull. Torrey Bot. Cl. 50:73.

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Schaffner, J. H. 1926. Siamese twins of Arisaema triphyllurn of opposite sex experimentally induced. Ohio J. Sci. 26:276.

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Worsclell, W. C. 1916. The "Principles of Teratology in Plants." vol. I I. Ray society. London. 49

Yampolsky, C. 1919. Inheritance of sex in Mercurialis annua. Am. J. Bot. 6:410-442.

Zhukovskii, P. M. 1940. Botanika (Botany). Second edition, p. 295. Moskva Sel'khozgiz. 50

Table 1. Factors known to modify the sexual expression of vascular plants under at least some conditions. Where more than one worker has shown sex reversal for a given species under a given kind of treatment, we have cited pertinent review articles in order to minimize the table's length. An asterisk indicates dioecious species. Nomenclature follows Bailey and Bailey (1976).

Table 2. Dioecious species known to change sex or produce hermaphroditic offspring. We have perhaps included some uncommon mutants on the lists, but the paucity of the literature treating sex reversal under field conditions makes it impossible to determine which species, if any, should be excluded. We have included species which the taxonomist may regard as rnonoecious to dioecious only v:hen such species have been reported to have sex chromosomes (e.g., Mercurialis annua, Jlex sp., or Empetrum nigrum) or when the rnonoecious state appears to be related to the reversal phenomenon (as for Arisaema triphyllum, !:::._.dracontiurn, !:::._.Japonicus and some of those listed in the Orchidaceae). An astrisk designates species reported to have sex chromosomes (Allen 1940, Westergaard 1958). 51

TABLE 1

Fc1ctor f)j,·:ct ir·n --··~---·-·- ,; AGE (S Fi:) (1 _,.. n Aris~1c11 1:1 dr~r-nnt·iu:"i;_ (L.) Schc;1t" Hes] op--Ha:!·r St>11 1 ~,1~~7 " ":._. .i"'l'"lli':::~ J:L.' j~e~:1op--'.l,'lrr >i\)Jl 195? (_ . .!!_:~l"'l)~1__!.u_~_\ (L.) T~rT.·r. 1-icslop-~!cirT sor, l~)s·i II ca~t·tlJu~~ e];~:,t:l~·-:1 u-:c•:-.:_/~)k DcL~qY(L~·.i.dize l~!(,~~ t!

II ., C~"cnoch.:s dt:ns~ flcru;;, H~1lfc* Crcgg l'.4/:, Lucco11:i: l''li-::Jidc·:, D. Oli•:cr·>· Dzl·1.:-i113:~jdiz-; 1963 i\,n M\L POP./,\0\i· S Fcrnal, .. 1 Oe~t'ro:~f! C5+ .,.Q SDcnc ,1:ioic;; (L.) Cl,1irv.* Ic,ve 2.nd L(Y1.:e 1910, 1~\:::S Ocstr;,:'. ic l " s. dfric:1 (l..J C:l:lin· . .,. I.o-ve anJ Le·,_;c J~),10, lJ·iS OesL:r,tc~]oJ rcu11i,.1;:~!lr:: S. cViojc;1 (L). CJajr\·. 7-- M,;.Jc 1 '1' (!:~Lu:: t C·l '\):-: C (J ..:- ~)

'i cs1 (1 ~-tP J_ \!t:L· " S. dioic;: (:,.) C:Jairv.* d-, y l ,. * " C:-1re::-~ ·:-1>. Crcrr J ~17~ Cllc.'i~::·js sJt:i.vJ r HcslOj)-IJa1·r~scn J~l57, " !~1innif~ J s3g " ll8slop-\L,n :. .c·Jn j 9:,7 BORON cf-<-0-, HNic.h 1 S'.i6 ,J !_J•> C;..n1r:;.:}·,]_.-1 s:1 ti_ v:,1 I * H,:,,;l op--ihn: i son 1072 Cur.:u11:·i:.... ~<·~c.>-::; l. ],i-;_nnin [1 Ty·: 1 j D:t 194 7 " ---- ·-·---• ·-·-··--~-- " !\i:·:rct.u·i.:, :: j s a:ql;_l2,11c.1._L. He~;J op- l-L::._.c:r1 s·~} ;1 l ~)'?'2 COLD 1'.'EATllf:R d-<- Atrjp}cy can•-~sl--:cns Pursh:-- H:trthnc l!:'iS 'I-' 7 " Cycas. ~--~!-~~jji:-1_"!_}_~_L. f,1cnr.i;1;~c~· 1 ~J67 DR(HJGlrr d+ Acc~r s~cc1 1~·1 ·,,·n !,i:.rt'S11. R:iri:t·:.· c ..t:. ::J (j!, :n·C:r{ir0-:.ic,n) " Cu,:t111:i,;· :;:,. :, L. ~Jjnni;i 10:,2 " Tr5tl·--- ni1 :tr·stj_\-U\\1 L. ~linni:, 1!lS2 ETIIYJJ;,L (uCUEii'·· .satiVQ 1,, Gregr, 1973 d

TABLE1 (continued)

F<..1.CTOI' J;cfc>rcncc

'f'jllct.i.,1 huchJ oear:a Budilol' d::irty1oitks (:~utt.) ll\J1''.;clell J9j6 l:J1gt;lu.' ... llcslop-Jlaj'rison 1924 Ustilago caricis Care•. pr;1ccox J~H:(1. nee. -S( hrcb. - l\'or5;ckl 1 1916 U, ~dlt]',:-:1'JTd.l'l Si Jc nc· ~1J La !11i J 1 . * llcsl()jJ• !lari:j '.·,on 19:;7 " (',, U. jTlf.1y- 0 K:1l:J;11..'.11c-c:!ntcr;:ra Medic. + (K. cren,,ta). Cntarino J.~\.>i

d-, C) C0t:.1 :-:-et1rn~(>\·pnn~~F:'. f!cJ-it15_f.* + 1~'-'.--~~-j j( " t~-_---!t!:.:-1; 1=-11\·1J~1---r1,-:)i c 11 (: x Kuth·, Grcr;g l 9i 3 II C. JJ11c·.c<_)(·!_o~.s_:rnRc1·,l)i_ f* C1'C[;g 197:~ II C. vcncr:i ~~,:..:,n":i)~:,tc:::. ·k Gregg 1,!73 " C. dc·n.;;-j fJ oJ~:..-·r: ]~oj fL,* Grcge 1~173 c:y110-l~j;~;:-tn-i;-l~-~-'.-1'1:1']-, ·~ ·~ f ·k Gregg 1 9/ ;:, II C~ ~Stt~lt(H1::C1 ..)'jt~i. ~)•._·]i]tr~?.· Grcgr 1973 " Cuc1n·l1 ~; s:1t j\·a L. Crc.gg 19/~5 " 1:5i(.-r::.--·r1.llTt1·;·11-,~~:n~;i ,1;~cq. Gregg 19'/:~ d,- ,·() I·~r1)_<1_1~c~1'.:.~f'_(i~r)'~Jj),c\. J_liu;) sat:iva I...-;- Schaffner 1921 " llu,:•:llus japoniCllS S1c·bolci & Zucc.• l-leslop--Horriso;1 l\!57 " Tl.:i l i <:.1:n!!:J c1asyr;:,,··rt:,i Fisd1. * f; ,\,•e--L:, 11 . Schaffner 19253 " T. cViojc\lin J,.* Sch3f:fncr JCJ2Sa METllYLr;c llLUE c( ?. Cui:bit;, sativa L. Dzh.Jp:iri

~; Bcp,oni3 se1111wrflorcr,:, Link & Ctto Hatzkc 1938 II c~n·:H:--\bis sati\ia L. * !Icslop-!larrison 1957, 1964 1! C•r: 1 t011lcrL; tkJ1 ic1 ..n1jdcs (L.) Rn,nrn. (g.:1;:c·topl!ytc) O~h8paridize 1963 II CluJ1:1cJ :;pino,a ,l:,;_q. M11rncek 1927 ti ti1-C~i::1~ ·s --;.il1tti'{):~~1L. l!C'slop-Ilarrio-

TABLE 1 (continued)

F;1ctor !)j rcct ion

NTTROGrn d., ~i Lycopci~s:!cu1!1 C'sculc-11tu1:1 r.!i1ls Heslop--H:1rrison 1972 II 6s1'.;i_ti'!J:1 __cj:i:._~-~:?. L (g~Jirlct 0- ,. f)7,h~1p,1r.idizc J 053 Zc~!_!:~•~y:~ L. lle!;lop-l!a~-ri so;1 J

Pl JO'J'Ol'LRJOD 1· LONGDAY 0 -<- y Cann~d•i s s~t:iv:i L. llcsJ.op-J!~~r:-i~ison 19~:7, 1972 " CUClll\ti.'.:;. -:!TtgP j J.~:, L. Hall 1,:-19 C1.1cur1i ~.~~n:·jya-- L. Heslop-Ihrri,;cm E>S'/ " lktt·:op,,;o::_ co1,tort,:•,_ (L.) l;cauv. ex R. f1 S. Totliill :rnd Kno:: J %;1 " 1itl':1ulus :i,tpon i cu•; :C.icbolcl f, Zucc." fle5Jop--llard_,:on J9S7 " X;:n11 hi lll\ 1• strl_~'..:<•Tit:1:1 L. lleslop-}hrT.i·-.011 J ~l'.,7 "

SHORT DX\' c!.,~) Ai:1b-:·o·;jc1 c1rtc-1:1j~-tfo]i:-: L. (A .. ch,t_i•Jr L.) " A. trjfi::1·1 L. Hes] op-IL: rri ,.on } :~:;7' II C:.1n11~\;i !. ·;·1ti,,' L. ,. Heslop-- H:1.I' .r i_~0n 19:;7, Cu, lll'[;,-t;:_ rc·;'CJ_! .. Jles1op- ll'ln .i5on E 1:7, 1,.-.,., .. _ ,, Ct:Cl!':-d !> .;:tt j_,,.-;-7_L. Hes J c)p--1IJ:.~t i sc•?: 1 ·JS 7, ~t·_~!~:~~_r)_:·,.·~_(?_!_!_ .c;)l' :·?~~t_l!:~ ( L. ) };C-?.1i'.'. t'X 1~. ti S. lkslcp-flarrjco:1 ]9'·7, ]97.: II II11>ulu:; j 8 pn_n i (~1 1.::. s-1 t:1,old & Zurc,* l!oslup -!1,t1'ri son 19~,7, 1, 0·.:2 II Sj J enc, pv.J11J ;: I.. !!eslop-lbrriscm 19:;7, 1(!72 II Spj n:_~-l_i ;1 ol c·~-a~:c;-io L. * lies] op-I brr i5c,11 19:;·/, J c1:,2 II Trlt i :.._u,:1c:cs~.ivL:.,·1: L. Jleslc,p-Harrison 19S7, 19·;;, II Xc1nt.Li1,nl pcn:1.syJ \'~:.nicuni W:1Jf\,. licslop-h3rrison 1957, 1972 II X. ~;tru·a;triu:n L. HcsJop-!larri,con 19:;7, 1972 II !lcslop-ll:i.rrison 19'.:7, 1972

POTASSJ t:;,! c!.,,.Q Dz.haparid'Lze l 9G3

11 R1CII SOlL" c!.,(~ Aris,,c-1:1'1 t.-i.niwl l•1r.1 (L.) Torr.'· ·' l-lcslop-llarrison 1 'lS 7 II A. dr,1~cnti\l1:1 (L.) Schult.* HcsJ op-Jl;in·i son 1957 II Cucu::,i ',ativ0 I. Dzh3pJridi:c 1963 II DzhapariJlzc 1963

d,. J\ml1n,:-i~ trif·id3 L. ¥ Cilni1Ji,, ian~tns (Tkmb.) Mat•;t::: f, -~:,Lai !lo:,) OJ'-lbrrl ;,Oll 1957 Ct1c-!1r;· i t_,1 pep() L. IiL~sJ Oj,-!l;1rri.sui1 1~1~,7 i:.'.tic~,;;,:,;_·-;,cti..1,:1 L. !Ir· s l Th:-):1;pson 195S 54

TABLE1 (continued)

I) i rcct ·j ,,n

:cu:o\'al c,f" lc~:-1 ve:-, d,_9 c:~-1nn:il)is :,:;t iYa L. -;.- Dzhapar:l Ji z.c ~;63 o~· fl Oh"r• J. 5 or II Car J ca p:-q1Zt:·ri_ L. * D:J1;1pt1r.i t~ i :.c :":S\. cro~•,in p::.·un_i_11p, ·llcslop--li::r,· ~01, ) 9,,-, II Clcom-~ !~rd11i.._::__~:1J~~.cq. llcs)o~)-!t~rrj s'_.,n i:1~·,7 II Cucx·,,,·( s :·::t.i \·:1 L. Hcs]op-!i:.1-risor, l:l~-7 ~L.'ec<)1· i-(1 J ·is· :inuu~t L. * H<:'~}np--tl~Lrr.i~cn l~JS7 II !,:orus- ~1 ! b~J J,. ·o: D:h3parldi:c Jijfi3 1l Hcslop-l~:-t1·r.is-:;;1 J jnjtff)" t(, J[l:!iE c.t .((' Acc_r n::r tinl-1c1 I -;- \·;ors,'cll }ClJ6 II cixj s or l:u f.C- ~-~_0_ L. D2har~riJi1.e 1963 br<:l11ch re:·,,c,va I of d,- (L.) Schott , ->- Bc·slop-JL1.:·r.is(;:1 1~1:·.7 11 {1. ;i_tif_'}_1]_~ DL • -;; He~;lop-lt.!.~·;· j :~c:•;: lS·S7 11 A. tr}11112_'_Jlt.!:!(L.) To1..-r.* 1!:csloi;-rb:,·.i~r,;1 ViS'i 55

TABLE 2

Ara c·,_

Sc:Jr:1.ffnc-r 1921, 1g2:-;0., J92~c, l~!~:~> l~3J, !Ijr..:U, l'l'.'·1, 1-':f'hec 1:1::'A 1-lc~(:,[tw:J 1~>2:"J~Jiuhnt~c 1.,;t. al 195(), Sc11~;1·,ush 19:,2, lksJop-11:trrison 19(,',

Sc.h:,ffnc·i· 1023b, Tournojs l~lll, 191::', 191;

5i]cl!c (Lyclini.s, ~-!:_,J211clrit..:1n) c1 1 l.1: 1 1'. -;; lly 18S2, SchuJJ 1~)11, Love ]::;-~o, 1045 7 S. --(f.i z::ca ( L. ) C 1 a j 1 -; • · Sc.hu 11 ] 9: 1, Lo\·c 19L:0, l ~l45 S-. ?tcl 9:-;~: S. roc-,.. ~r; l"r.in. Cor1cns 1928

/\trjp] '~':( c:1:-::c~~Cl'J1.S Pur.~h. i

J\,1tcn11ciri:1 ,i:ioica (L.) G:,ertll. iJt' s,,h J9y; (:{y~-.-rl.1·:1·:trv-c•n·;~, (L.) Sr~o11. C-:,r,:cr,'.'- 111::8 !)L~!-.~~-~t(:~~ jtn?onicn_~ S.icr)old 4 Zucc. Ikc:no 1937

Cyc-acla c.cJ c Cycas c_irc_n~~,Jjs L. itenningcr 1967

Bl ;::ckhunt 1938

llz},:ipr, jdizc l 963

Eu::-.onr::i1 t111,1oj(lc:; n. Oliver lhh:ipur id i ze 1963

EUJ)horhi_accac Y:mi,o1sky 1919, G,ibe 1939, Kuhn 19:59 56

TABLE 2 (continued)

Reference

Rjck nrid I!:n1n.1 (19-,:~)

M\\ r ~:c C<"ie C;;sti l1on cl :,rti en Sc.ssc J\osse 1 ~1:~s Sc-haffi;cr 192S<1, Zhu\;oyskii 1940, lhh:1p:!rid:izc l9G:,

Orch:i.tlacC'de Ci,t;,,,ctuu C'J''lll:··,·, lkhb. f. Gregg 1 "7:5 C. r.·:icroc:,,iJi:_;·,, I~. ·i:. Rjch. ex. K1:nth Gregg J 0 7:~ C. r1,'"lcr~1rJ_(~s:.-.!1::r!)c-11!), f. Grc 1:r. l (; :, C. y,_-:11·rj co~:11·1; lt:tc11!. Grq:g J 97:5 Cvc1i(

l'ior:.d< ! !. l 916

bu.::11loc J; 1 r_:t~._·l0i1lcs Xutt. Worsdel_J. 19]6 !,<'UC12JXJ;J- t ~}\,:.i. S. \};1tt S Harpe_!', Freeman t; ?,ic-,\ri 1nn" (pcrsc-11~~l o b:-:crv?. t ion)

Putwai11 i; 11:n,wr 1072, Ono l c,3J R. c-1 ~:,·tosclJ~1 J * Put\':~~iri I; i!~d'j)()I' 1~)72 ------Ru~cl)t in. sp. Mcnn.i.11::e:r J ~i6"/

]J_~~]__l_c:~]~~-~-(~cL,.sy~:(.:-c21rn Pi sch. 6 /\'I'll- Lall ScJE,ff;:,,;- 192'.,a, Ku!,,1 1°39 T. dioic:i L. Sch~ffncr 1923a, 1925 T. f;:j;-Tfi:~ri Engclrn. ~cl1affncr 1923a, 192S, Kuhn 19:=i9

Fr;1 g:n_i a (po 1yplo.i d s) Lilienfcltl 1933, 1936, 1936b Scb cmanr, 1931

Sal ic~cc::1 e T'C:Jllllus trc;:mloiclcs Hiclix. * El·l:ins:;on (; llnma;1 1927 Salix ~=p. Nilsson 1918, Raino 1927 s·iiYTX-nJba L. llcslup-11:nri son J 924 S. ar~i c~r•;on i .i. Sn.* J:,_-.s]cp-H;~rrjson J:)2,1 S. aurita L. ·• lfor.sddl 1016 s. c::1 r~rc·a J..* licslop-11:n·rison 1924 S. ci ncn.:a L. '' Jlcslup-ll:1n·i son 192,1 S. ~~ri1-1(f~i7"0l i :1 St 0 r .i Ti£c !lcslop-!!ai-rjson 1924 S. silesi;;ca \\'i.lld. Heslr, 11-!l~norison 19:-!4

Taxus hnc-cata L. Keen f, Ci::i,!wjck 19S<1 'f. cusj1ida Sd.chul,l (; Zucc. Keen 4 Ci1;1 ,h-1 j Ck 1%4 T. mcdi:! Fc'hd. Keen G CJ.ad1·:ick 1951

Url~CJCt'3C Urt"ic;i c-ann:1l,in:1 L. NPgod i. 1~.i57 · U. c-~n1d:1t'.'J \:~1hl. ~e,:od_i_ lJ2~l u. diOiC3. L<· S, ra,;h'.!l'gcr 1910 57

TABLE 2 (continued)

Refc:rcncc

V:11crj a Ni c:c<1c· Corrcns l ~128

Vitaccac Vi.tis (1·:ilc: populJticn of sevc,r-:ll Nq;rul J 936, BrcicJrr- f, Sdwu 193f;, -Sj)C.ciC'S arc d-·!:<-~clous. Tl:c IIedrick cnjci Anthot1y J 9J_5, c:,1lt.iv~1tcJ t1L·ri.10pf-:roditc:s hsnte Negi avd Olmo 1965 bC'e:a1se] cc:t.c,i f1·o;n ,-:ilcl 5--tcck. (All en l Y·.O) ------·------1. l}cx PLANTDIOECY: ECOLOGY,EVOLUTION AND SEX REVERSAL

D. Carl Freeman

Department of Botany and Range Science

Ph.D. Degree, August 1977

ABSTRACT

The distribution of dioecious species among forty-four plant communities of western United States was examined. The dioecious habit is most prevalent in harsh environments. In many communities, over 20 percent of the species and 40 percent of the individuals are dioecious. Dioecy is most common among woody species which are pollinated by wind.

It is concluded that inbreeding depression alone is insuffi- cient to account for all known facts concerning dioecy. Disruptive selection acting upon differential success of gametes produced on sites of differing quality appears to have played a major role in producing separate sexed individuals.

Dioecious species reported to exhibit sex reversal and factors believed to promote such reversals are tabulated. It is concluded that for dioecious species which exhibit differential resource utilization by the sexes, individuals which produce offspring capable of sex reversal have a selective advantage. Sex reversal provides a strategy that permits dioecious species to reproduce optimally in patchy environments. COMMITTEEAPPROVAL: