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Labile Sex Expression in Plants

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Labile Sex Expression in Plants Biol. Rev. (1998), 73, pp. 157–180 Printed in the United Kingdom # Cambridge Philosophical Society 157 Labile sex expression in plants HELENA KORPELAINEN Department of Biosciences, Division of Genetics, P.O. Box 56, FIN-00014 University of Helsinki, Finland (Received 27 February 1997; revised 12 September 1997; accepted 30 October 1997) ABSTRACT The range of environmental sex determination and sex changes throughout plant taxa from bryophytes and pteridophytes to spermatophytes is reviewed. Lability in sex expression occurs in many plant taxa but only in homosporous pteridophytes is labile sex the rule. Among angiosperms, labile sex appears to be more common among dioecious and monoecious plants than among hermaphrodites. However, hermaphrodites can control allocation to male and female functions by varying the relative emphasis on pollen and ovules. A majority of plants with labile sex expression are perennials, which indicates that flexibility in sex is more important for species with long life cycles. Environmental stress, caused by less-than-optimal light, nutrition, weather or water conditions, often favours maleness. The extreme lability in the sex expression of homosporous pteridophytes is suggested to be related primarily to the mating systems. Key words: labile sex, adaptation, Bryophyta, Pteridophyta, Spermatophyta. CONTENTS I. Introduction ............................................................................................................................... 157 II. Bryophyta................................................................................................................................... 158 III. Pteridophyta............................................................................................................................... 159 IV. Spermatophyta ........................................................................................................................... 172 V. Conclusions................................................................................................................................. 174 VI. References................................................................................................................................... 174 I. INTRODUCTION the traditional morphological descriptions (Lloyd, 1980a). The functional gender of a plant estimates Sex expression is considered to have a strong the proportions of its genes which are transmitted environmental component when sex is determined through male or female gametes. Although estimates or changed at some point after fertilization. The of functional gender provide an ideal measure of the term sex expression refers here to male and female gender strategies of plants as sexual parents, they do individuals of dioecious plants, or to male and female not necessarily correspond with the actual success of flowers or gametangia of monoecious plants, or to a plant in leaving descendants through its male and hermaphrodism. Variation in the relative emphasis female gametes (Lloyd, 1980a). on pollen}sperm and ovules}eggs among mon- Why do various organisms then possess labile oecious or hermaphroditic plants is generally not systems instead of strictly genetic systems that included here. Sexually labile plants have the determine a fixed sex expression? Following the sex potential to have either male, female or both sex ratio model presented by Trivers & Willard (1973), organs, with some environmental feature deter- Charnov & Bull (1977) proposed a now classic mining which genes are switched on. However, such model to account for the adaptiveness of environ- simplified morphological descriptions of gender have mental sex determination in particular life histories. limitations. When analysing the adaptive signifi- They postulated that environmental sex determi- cance of gender variation, numerical estimates of the nation is favoured by natural selection when an relative capabilities of plants as male and female individual’s fitness as a male or female is strongly parents (functional gender) have advantages over influenced by environmental conditions and when 158 H. Korpelainen the individual has little control over which en- expressions within the same clone. Therefore, the sex vironment it will experience. The requirement for expression of sexually labile clonal plants is ramet- the evolution and maintenance of environmental sex specific and not genet-specific. determination is the ability to recognize an en- vironmental factor which differentially correlates with male or female fitness. Thus, labile sex II. BRYOPHYTA expression, through which an individual can increase its genetic contribution to future generations, is an Bryophytes are generally treated as a single division adaptation to certain life histories. including three classes: Anthocerotae (hornworts), Despite controversy over the adaptive significance Hepaticae (liverworts) and Musci (mosses). They of labile sex expression in plants (see Freeman, possess an alternation of generations in which the life Harper & Charnov, 1980; Lloyd & Bawa, 1984), sex cycle involves a free-living, haploid gametophyte changes appear generally advantageous and can be alternating with a reduced, dependent, diploid viewed as adaptations to patchy environments. sporophyte. Bryophytes are considered structurally However, some variation may result from the simple compared to vascular plants. Although inability of a plant to control its sex precisely in a bryophytes are homosporous, approximately 68% of complex environment. Such rare and irregular liverworts and 57% of mosses are dioecious (Wyatt inconstancies are hardly adaptive (Lloyd & Bawa, & Anderson, 1984; Wyatt, 1985). Hornworts are 1984). regarded as being approximately equally divided In the present paper, I review the range of between monoecious dioecious species (Longton & environmental sex determination and sex changes Schuster, 1983). In general, dioecy is considered to throughout plant taxa from bryophytes and pteri- be a primitive feature in bryophytes. The evolution dophytes to spermatophytes, and I explore the con- of monoecy has apparently occurred independently ditions that influence sex expression. Among labile in many lines (Longton & Schuster, 1983). Despite sex expressions, two categories can be distinguished. homospory, two ranges of spore sizes have been First, sex is influenced by the environment at some found in dioecious species (Chattopadhyay & point after fertilization. Sex then becomes fixed and Sharma, 1991). There is evidence that smaller spores is not amenable to further modification. Several give rise to male gametophytes and larger spores to studies have shown that such environmental effects females. Several species of dioecious bryophytes occur in a diverse range of animals (reviewed by possess distinguishable sex chromosomes (Anderson, Korpelainen, 1990). In plants, environmental effects 1980; Ramsay & Berrie, 1982; Chattopadhyay & on sex usually belong to the second category, Sharma, 1991). sequential hermaphrodism, in which sex is labile Although chromosomal sex determination is ex- during the reproductive lifespan. The choice of pected to result in a 1:1 production of male and gender can be made repeatedly or for a lifetime. In female spores, several investigations have detected animals, sequential hermaphrodism is a rare pheno- biased sex ratios in dioecious bryophytes (Wyatt & menon apparently because an early development of Anderson, 1984; Longton, 1990). Females outnum- fixed sexual differences enables an individual to ber males in most species that have been studied. better learn its sex role and become more successful Sterile gametophytes bearing neither male nor at mating and parenting. Despite the widespread female gametangia are also common in many occurrence of labile sex determination, the majority populations. Asexual methods of gametophyte re- of plants exhibit a fixed genetic sex expression, production are important in most mosses and in mostly hermaphrodism. The dioecious system with numerous hepatics (Longton & Schuster, 1983). It is separate male and female individuals is quite rare in also of minor importance in anthocerotes. Some plants, but is the rule in animals. bryophyte species have the ability to produce also Both genetic and environmental sex-determi- sporophytes asexually (Bopp, 1983). The rarity or nation mechanisms are sometimes found in closely the total absence of sporophyte production is usually related plant species, even within the same species. associated with the dioecious condition (Longton & Also, the degree of lability varies. In the case of Schuster, 1983). clonal growth, which is common among plants, Many monoecious bryophytes express temporal different parts of the clone (genet) may encounter variation in sex distribution (Anderson & Lemmon, different environmental conditions. If environment 1973, 1974; Longton & Miles, 1982; Shaw, 1991). influences sex expression, there may be varying sex In most cases, it is not known how such temporal Labile sex expression in plants 159 patterns in sex expression are controlled. However, b). The bisexual gametophytes of pteridophytes are there is some indication that environmental factors called hermaphrodites. Yet, a more appropriate have at least some effect (Table 1). In the mon- characterization would be monoecious, because the oecious species Tetraphis pellucida, sex expression antheridia and archegonia are produced in different is sensitive to density: male shoots dominate at locations on the same thallus. Unlike the other
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