Download Can classifications of functional gender be extended to all land plants?

Perspectives in Plant Ecology, Evolution and Systematics 14 (2012) 153–160
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Can classifications of functional gender be extended to all land plants?
Linley K. Jesson a,b,∗ , Phil J. Garnock-Jones b
a
b
University of New Brunswick, Department of Biology, P.O. Box 4400, Fredericton, NB, Canada E3B5A3
School of Biological Sciences, Victoria University of Wellington, P.O. Box 600, Wellington, New Zealand
a r t i c l e
i n f o
Article history:
Received 8 August 2011
Received in revised form 23 October 2011
Accepted 25 October 2011
Keywords:
Breeding systems
Cosexuality
Dioecy
Gametophytes
Hermaphroditism
Land plants
Sporophytes
a b s t r a c t
Land plants (bryophytes, seedless vascular plants and seed plants) may have combined or separate sexes,
and this variation also may occur at two life-cycle stages. Thus plants show variation in individuals’
attainment of fitness via sperms versus eggs (functional gender) and the diversity of gender morphs
found in populations. We extend D.G. Lloyd’s classification of flowering plant gender to all land plants,
with three main functional classes according to whether populations are dimorphic or monomorphic for
gender (i.e., populations consist of either one or two distinct sex classes), and at which life cycle stages
this occurs: (1) sporophyte-dimorphic, (2) sporophyte-cosexual and gametophyte-dimorphic, and (3)
gametophyte-cosexual. In dimorphic sporophytes and gametophytes, morphs that reproduce mostly as
females and males may be constant (dioecy) or inconstant (gynodioecy, androdioecy, trioecy). We suggest
that examining the sex conditions of seedless plants using a functional perspective will reveal a diversity
of sexual systems largely analogous to those found in seed plants. An extended suite of model plants
with different biological attributes will allow new tests of existing models of mechanisms that select for
different sexual systems, and may lead to important new questions in the field, some of which we suggest
here.
© 2011 Elsevier GmbH. All rights reserved.
From classification to function: the evolution of plant
gender
Across eukaryote lineages, some sexual organisms combine
female and male functions in every individual (gender monomorphism) whereas others separate them into specialized females or
males as a genetic dimorphism (and known in plants as gender
dimorphism, Darwin, 1877; Lloyd, 1982; Sakai and Weller, 1999). In
most animals, the position and number of gonads and genitalia are
determined during embryonal development, whereas the meristematic growth forms of at least one life stage of land plants provide
them with opportunities to vary the separation of sexual functions
in time and space. This allows variation in quantitative expressions
of gender and some controls on the extent of inbreeding (Darwin,
1876; Lloyd, 1976; Charlesworth and Charlesworth, 1987; Barrett,
1998).
Historically, classification of sex expression in plants has varied among the major taxonomic groups. For example, Linnaeus
(1737, 1753) focused primarily on distinguishing perfect (combining micro- and megasporophylls) from unisexual flowers.
∗ Corresponding author at: University of New Brunswick, Department of Biology,
P.O. Box 4400, Fredericton, NB, Canada E3B5A3. Tel.: +1 506 452 6025.
E-mail address: [email protected] (L.K. Jesson).
1433-8319/$ – see front matter © 2011 Elsevier GmbH. All rights reserved.
doi:10.1016/j.ppees.2011.10.003
Accordingly, conditions such as monoecy and dioecy, where plants
have unisexual flowers, came to be seen as deviations from a
perfect (hermaphrodite) ideal. Linnaeus (1753) grouped seedless
plants (including ferns and bryophytes) as “Cryptogamia”. Darwin
(1877) followed Linnaeus in proposing a range of terms based
largely on the morphology of flowers, but he introduced new
terms distinguishing systems that are monomorphic from those
that are dimorphic. For flowering plants, terms such as androdioecious, gynodioecious, polygamous, and polygamodioecious
(Darwin, 1877) have been widely used to describe a variety of
morphologically intermediate conditions.
In many land plants, sporophytes do not specialize as female
or male, but gender dimorphism can occur at the gametophyte
stage. Gametophyte sexuality of cryptogamic plants continues to
be often classified according to morphology (Anderson, 1980), and
a plethora of terms has arisen that is based largely on the morphology of individuals (Malcolm and Malcolm, 2006). For example in
mosses, instances of gender dimorphism and cosexuality are both
likely to be included under the poorly defined terms heteroicous,
polygamous and polyoicous. Malcolm and Malcolm (2006) treat
these terms as synonymous: “Heteroicous: produces various types
of inflorescences on different plants or on the same plant, so that it
confusingly seems to be both dioicous and monoicous”.
David G. Lloyd pioneered an understanding of the variation in
seed plant reproductive strategies from a functional, rather than
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L.K. Jesson, P.J. Garnock-Jones / Perspectives in Plant Ecology, Evolution and Systematics 14 (2012) 153–160
Fig. 1. An overview of plant sexual life cycles.
a descriptive, point of view, and simplified the existing terminology (Harder and Barrett, 2007). At the same time he drew
important functional and terminological distinctions between
phenomena pertaining to flowers, individual plants, and whole
populations. Following Lloyd (1979, 1980a,b) the key considerations are whether populations are mono- or dimorphic, the
proportion of fitness achieved by individuals via sperm or eggs relative to the other members of their populations (functional gender),
and the relative separation in space and time of their reproductive structures. Here, we compare what is known of the diversity
of functional gender within populations of seedless vascular plants
and bryophytes to sexual systems documented in seed plants. We
will treat herkogamy and dichogamy of seedless plants in detail
elsewhere.
Extending the generality of functional gender
All land plants have alternation of multicellular generations,
whereby haploid gametophytes alternate with diploid sporophytes
(Fig. 1). Land plants differ in which generation is responsible for
presenting gametes, at least in a functional sense. Strictly, gametes
are produced and presented by gametophytes only. The microgametophytes of seed plants are strongly reduced so that, in most,
they produce only one sperm that sires offspring. However, their
megagametophytes are retained within ovules and in angiosperms
these ultimately produce only one egg and embryo; even in gymnosperms where multiple eggs may be produced per ovule, almost
always only one embryo matures. Thus, gametophytes in seed
plants can be considered functionally equivalent to gametes even
though they are produced by spores and presented by sporophytes.
In land plants, both gametophytes and sporophytes may have
combined or separate sexes, and their gender is quantified by
their relative contributions to the next generation via female or
male gametes or spores (eggs/megaspores or sperms/microspores
respectively). Because all land plants have fundamentally the same
lifecycle, and selection acts on both gametophyte and sporophyte
stages, theory developed for flowering plants can be extended to all
land plants. Additionally, because seedless plants have free-living
gametophytes that vary in their sexual conditions, and these gametophytes can be easily manipulated, we can ask questions about the
role of gametophyte selection that are not easily addressed using
seed plant model systems.
The expression of gender in land plants
Three gender conditions exist in land plants (Table 1). First,
plant populations can be monomorphic at both the gametophyte
and sporophyte stages (e.g., many mosses, liverworts and hornworts, Lycopodiaceae, and all, or at least most, homosporous
ferns). Secondly, they can be dimorphic at the gametophyte stage
but monomorphic at the sporophyte stage (e.g., gender dimorphic bryophytes, perhaps a few homosporous ferns, Selaginella,
Isoetes, and all heterosporous ferns and sporophyte-cosexual seed
plants). Within this class, the gametophyte can be free living or
endosporic, and the relative sizes and longevities of gametophytes
and sporophytes can vary. Thirdly, they can be dimorphic at both
gametophyte and sporophyte stages (e.g., gender dimorphic seed
plants) (Fig. 1). Our terms gametophyte- and sporophyte-dioecy
are equivalent to haploid- and diploid-dioecy of other authors (e.g.,
Bull, 1978; Bowker et al., 2000), but we prefer them because in
bryophytes changes in ploidy can be associated with changes in
gender (Crawford et al., 2009; Jesson et al., 2011). Thus we can
avoid confusing two issues in terms such as “haploid-dioecious
diploids”.
Gametophyte cosexuality
Cosexual gametophytes are of one type that produces both
sperms and eggs. About 50% of all bryophytes are gametophyte
cosexual. If the gametophyte is cosexual, the sporophyte is effectively genderless as it only produces one kind of spore (homospory)
that gives rise to cosexual gametophytes. This is found in many
bryophytes (e.g., Physcomitrella, Chonecolea, Dendroceros), many
lycophytes (e.g., Lycopodium), Platysoma, and most homosporous
ferns, but is absent in seed plants. All homosporous ferns have
the capacity to be cosexual, although epigenetic control of gender through antheridiogens occurs in a number of fern families
(Korpelainen, 1998) and so sex expression is environmentally
labile.
L.K. Jesson, P.J. Garnock-Jones / Perspectives in Plant Ecology, Evolution and Systematics 14 (2012) 153–160
155
Table 1
A classification of the gender conditions found in land plants. Spores and gametes can have similar or different morphologies (isosporous and anisosporous respectively).
Sporophytes
Spores, gametophytes,
and gametes
Conditions
Gametophyte cosexual
Gametophyte dimorphic and sporophyte
cosexual
Sporophyte dimorphic
Individuals genderless; populations
monomorphic
Individuals cosexual, populations
monomorphic; isosporous,
anisogamous
gametophyte gender diphasy, etc.
Individuals cosexual; populations
monomorphic
At least some individuals unisexual,
populations dimorphic; isosporous or
anisosporous, anisogamous
gametophyte-dioecy;
gametophyte-gynodioecy;
gametophyte-androdioecy;
gametophyte-trioecy;
sporophyte-monoecy, etc.
∼50% mosses, ∼40% liverworts, ∼80%
hornworts, Selaginella, Isoetes,
heterosporous ferns, 90–93% of seed plants
Gametophyte-gynodioecy: Atrichum
altecristatum, as described by Anderson
(1980). Some plants are constant female.
Inconstant male plants are strongly
dichogamous such that male and female
phases happen in separate years.
Gametophyte-trioecy: In Pogonatum
microstomum polyploid populations have
mixtures of hermaphroditic, female and
male plants, whereas the diploid
populations are gametophyte-dimorphic
(Sharma, 1963)
At least some individuals unisexual;
populations dimorphic
At least some individuals unisexual,
populations dimorphic; anisosporous,
anisogamous
sporophyte-dioecy;
sporophyte-gynodioecy;
sporophyte-androdioecy, etc.
Examples
∼50% mosses, ∼60% liverworts, ∼20%
hornworts, Lycopodium, most ferns
Examples that warrant
further investigation
Gametophyte-cosexuality through
rhizautoicy: Aloina bifrons, male and
female ramets of the same genet
connected by rhizoids
∼7–10% of seed plants
Sporophyte dimorphism through sex ratio
distortion or spore abortion: In
Macromitrium four spore sizes occur,
corresponding to females, aborted females,
males, and aborted males (Ramsay, 1979).
If all one spore class is aborted in a single
sporophyte, then this would functionally
be sporophyte dimorphism. While there is
no conclusive evidence that this condition
occurs in seedless plants, in Ceratodon
purpureus there is a genetic component to
sex ratio distortion, likely due to
chromosomal interactions (McDaniel et al.,
2007)
Gametophyte dioecy and sporophyte cosexuality
Monomorphic populations
Gametophytes in gender dimorphic populations specialize to
produce either sperms or eggs (e.g., all seed plants, a few seedless
vascular plants such as Selaginella and Marsilea, many bryophytes).
Cosexual sporophytes produce both female and male spores (since
the spore is simply the first cell of the gametophyte, which
will either be female or male). We refer to this as heterospory,
regardless of whether the male and female spores are equalsized (isospory) or unequal (anisospory), following Bateman and
DiMichele (1994).
It is likely that gametophyte-cosexual plants vary in their individual success at contributing genes to the next generation via
sperms and eggs just as sporophyte-cosexual seed plants do (see
Webb, 1979; Lloyd, 1981; Garnock-Jones, 1986; Wells and Lloyd,
1991), but we are not aware of any data that could be used to
demonstrate this.
Many homosporous fern gametophytes show changes in sex
expression over their lifetime (gender diphasy). The ontogenetic
sequences vary and can change from male to hermaphrodite, from
male to female to hermaphrodite, or from female to hermaphrodite
(Klekowski, 1969b; Korpelainen, 1998; Quintanilla et al., 2005).
In this system, the relative contribution via eggs and sperm will
change as the individual grows, and so individuals in different
resource environments may differ in their contributions from one
or other sex function. Some authors have described populations of
dichogamous homosporous fern gametophytes as dioecious or trioecious. For example, in Culcita macrocarpa populations consist of
males and hermaphrodites, while in Woodwardia radicans, populations consist of females, males, and hermaphrodites (Klekowski,
1969a,b; Quintanilla et al., 2005). However, the sex of these plants
varies over the plant’s lifetime (Klekowski, 1969a; Quintanilla et al.,
2005), so individuals on average will gain half their fitness via
female function and half via male function and so are cosexual
(Lloyd, 1980b). In Equisetum, gametophytes may be initially unisexual, but females and sometimes males may become bisexual
with age (Walker, 1937; Duckett and Duckett, 1980; Duckett, 1985;
Guillon and Fievet, 2003); it remains to be shown whether this is
a leaky dimorphic system or a monomorphic system with strong
dichogamy.
Gametophyte and sporophyte dioecy
Sporophyte gender dimorphism occurs when sporophytes specialize in their spore production as predominantly female or
male. All known examples of sporophyte gender dimorphism are
seed plants, and the condition has arisen many times independently (e.g., see Weiblen et al., 2000) although the majority of
seed plant species (∼94% of flowering plant species, Renner and
Ricklefs, 1995) have gender monomorphic sporophytes. Although
in some seedless plants (e.g., Selaginella, Marchantia, Ceratodon)
the gender of spores is determined before they leave the sporophyte, as far as we know none has developed sporophyte
dimorphism.
The range of functional gender in dimorphic and monomorphic
populations
Because gender is a quantitative phenomenon, plotting ranked
estimates of phenotypic gender (e.g., the relative proportion of
female shoots, archegonia, etc.) can help to determine the number
of sex classes that occur in the population, providing information
on the range and diversity of sexual systems that can occur in land
plants (see Fig. 2).
Dimorphic populations
In sporophyte-dimorphic plant populations, there can be variation in the degree of constancy of the female or male sex. In
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L.K. Jesson, P.J. Garnock-Jones / Perspectives in Plant Ecology, Evolution and Systematics 14 (2012) 153–160
Cumulative proportion
1.0
1.0
(a)
0.8
0.8
0.6
0.6
0.4
0.4
0.2
0.2
0.0
0.0
0.0
1.0
0.5
1.0
0
1.0
(c)
0.8
0.8
0.6
0.6
0.4
0.4
0.2
0.2
0.0
0.0
0.0
0.5
1.0
(b)
0.5
1
0.5
1
(d)
0
Phenotypic gender
Fig. 2. The relative cumulative proportion of female shoots (phenotypic gender) in greenhouse populations of mosses (a) Bryum lisae and (b) Barbula unguiculata measured
6 months after isolating single germinated spores; (c) Bryum lisae and (d) Barbula unguiculata measured 14 months after single spore isolation. Gametophytes were grown
from single spores of sporophytes (10 and 15 sporophytes respectively) collected from a natural population. All fertile shoots in a gametophyte were scored for presence
of male, female or bisexual shoots. Bryum lisae is gametophyte-cosexual. In this species, antheridia (male sexual structures) are produced before archegonia (female sexual
structures), and so initially some plants were recorded as having only male function, but became simultaneous hermaphrodite throughout the year. Barbula unguiculata is
gametophyte-dimorphic, and individuals are either male or female.
dioecy, both gender morphs are constant. Thus some individual
plants transmit genes only via microspores whereas others transmit genes only via megaspores. In gynodioecy (Darwin, 1877; Lloyd,
1976; Webb, 1999) the male gender is inconstant, with all producing pollen but some or all individuals producing some seeds, while
all female individuals produce seeds but never pollen. In the rare
condition androdioecy the female gender is inconstant, with some
or all individuals producing some pollen, while all male individuals produce no ovules (Darwin, 1877; Liston et al., 1990; Pannell,
1997b, 2002).
Analogous conditions likely occur in gametophytes of seedless plants. The presence of females and hermaphrodites
have been recorded in Platyzoma (Tryon 1964), Atrichum altecristatum (Anderson, 1980), Atrichum undulatum (Jesson et al.,
2011) and Luisierella (Eckel 2007), suggesting the possibility of (gametophyte-) gynodioecy. Additionally males and
hermaphrodites may perhaps occur in Sphagnum quinquefarium
(Smith 1980). In the moss A. altecristatum, first year gametophytes
express only female or male sex structures such that young populations can appear gametophyte-dioecious. However in their second
and subsequent years, these plants are female. Based on lifetime
sexual performance, this species appears to be gametophytegynodioecious, as some morphs are constant females, whereas
others start life as males but then become females (Anderson,
1980, Jesson et al. unpubl. data). A similar pattern occurs in A.
undulatum s.l. where females produce female gametangia consistently each year, while hermaphrodites are either simultaneous
hermaphrodites, or produce male sexual structures in one year,
followed by female sexual organs in later years (Jesson et al., 2012,
in press).
Integrating plant mating system theory: extending
questions through new model systems
Extending models of the evolution of selfing and outcrossing to
gametophytes
While seed plants and bryophytes that are gametophytedimorphic and sporophyte-cosexual experience the same types
of selfing (intergametophytic selfing or autogamy), simultaneous
hermaphroditic gametophytes can have an additional level of
inbreeding: intragametophytic selfing (or automixis). In intragametophytic selfing, self-fertilization occurs within a gametophyte,
where sperms fertilize eggs on the same gametophyte. Gametophytes produce gametes by mitosis. Thus, in the absence of
mutation, sperms and eggs from a hermaphroditic gametophyte
are genetically identical and selfing produces zygotes, and eventually sporophytes, that are homozygous at every locus. (It is
interesting to note that despite apparent genetic uniformity,
there is considerable morphological and physiological variation
in spermatazoa within an individual and in gametophytes produced by intragametophytic selfing; Shaw, 1990, 1991; Renzaglia
et al., 1995.) It has been predicted that intragametophytic selfing
results in faster purging of genetic load at the sporophyte stage
than through intergametophytic selfing (Klekowski, 1979, 1982;
Hedrick, 1987). For example, simulations by Hedrick (1987)
L.K. Jesson, P.J. Garnock-Jones / Perspectives in Plant Ecology, Evolution and Systematics 14 (2012) 153–160
suggested that genetic load in homosporous ferns that reproduced
primarily by intragametophytic selfing could be 0.5–0.6 of that
for ferns undergoing intergametophytic selfing. This suggests that
in gametophyte-cosexual species, inbreeding would be an evolutionarily stable state, as has been shown in seed plants (and see
Lande and Schemske, 1985; Barrett and Eckert, 1990; Goodwillie
et al., 2005). Despite this, mixed mating is common in ferns and
mosses (Klekowski, 1982; Soltis and Soltis, 1987; Eppley et al.,
2007; Wubs et al., 2010; Jesson et al., 2011), and theory developed
to explain the predominance of mixed mating in flowering plants
(reviewed in Goodwillie et al., 2005) can be extended to include
gametophytic life-stages.
What is the influence of the gametophyte stage in the selection for
combined or separate sexes?
Theory suggests that a male or female mutant can invade a
hermaphroditic population when self-fertilization causes severe
inbreeding depression, or if the benefits of reallocating resources
to specialize in male or female function are high (Darwin, 1877;
Charlesworth and Charlesworth, 1978; Charnov, 1982; Lloyd, 1982;
Charlesworth, 1999). Inbreeding depression should be a strong
evolutionary force in all cosexual plants (Klekowski, 1969b, 1973;
Scofield and Schultz, 2006; Taylor et al., 2007). In addition, in
polysomic polyploids, inbreeding can lead to deleterious effects
in the gametophyte (Butruille and Boiteux, 2000). The amount of
inbreeding depression experienced by sporophytes can be reduced
if there is high overlap between genes expressed in both sporophyte and gametophyte and deleterious alleles are purged in the
gametophyte (Charlesworth and Charlesworth, 1992). For example, in the moss Funaria hygrometrica, 75% of genes are expressed to
some extent in both gametophyte and sporophyte (Szövényi et al.,
2011), suggesting many deleterious mutations will be purged by
expression at the gametophyte stage, reducing inbreeding depression in the sporophyte stage. If avoidance of inbreeding is a major
force selecting for separate sexes, strong overlap between gene
expression at gametophyte and sporophyte stages would lower
selection for separate sexes in gametophyte-cosexual populations. However in some gametophyte-dioecious mosses inbreeding
depression in the sporophyte has been shown be considerably high,
suggesting that strong genetic correlations between life stages may
not purge all genetic load (Taylor et al., 2007; Szövényi et al.,
2009).
Because gametophytes of seedless plants are nutritionally independent of the parent sporophyte, and are easily amenable to
manipulation, they can be used to experimentally test theoretical predictions about the role of the gametophyte in purging
inbreeding depression, and reducing the selective advantage of
separate sexes. For example, if deleterious alleles have a higher
fitness cost in harsh environments, purging of mildly deleterious
alleles may be environment-specific, ultimately resulting in gametophytes in harsh environments experiencing less sporophytic
inbreeding depression than gametophytes in benign environments.
This would predict the fitness cost of inbreeding would be greater
for sporophytes in benign environments or sporophytes in newly
harsh environments, and a correlation between mating system and
environmental stress.
Testing hypotheses of the advantages of diphasy over dioecy
Diphasy occurs in approximately 0.1% of angiosperm sporophytes (Lloyd and Bawa, 1984), and considerably higher ratios
occur in fern gametophytes. The advantages of diphasy and gender
dimorphism are similar, and include obligate outcrossing and
predator avoidance (Cruden and Hermann-Parker, 1977; Thomson
157
and Barrett, 1981; Lloyd and Bawa, 1984). The advantages of
dioecy include limiting dramatic sex ratio fluctuations, as the
sex ratio is determined by a binomial distribution (Bull, 1980),
minimizing the fitness costs of changing sex (Charnov, 1982),
and reducing a need for a mechanism in plants to accurately
assess their environment (Lloyd and Bawa, 1984; Zhang, 2006).
Conversely, diphasy can allow for easier exploitation of favourable
circumstances experienced by a plant (Charnov, 1982; Lloyd and
Bawa, 1984; Zhang, 2006), especially if there are different relations
between the fitness of each sex with mate availability, resource
level, time, size, age, or developmental stage (Ghiselin, 1969;
Charnov, 1982; Lloyd and Bawa, 1984; Day and Aarssen, 1997).
Most homosporous ferns are not strictly diphasic, and have a
hermaphroditic phase. This suggests that reproductive assurance
may play a role in maintaining the sexual system (Baker, 1955,
1967; Stebbins, 1957; Klekowski, 1969b).
Experimental tests of hypotheses selecting for sex-switching
versus constant gender dimorphism should be possible using
homosporous ferns as an experimental system. Research elucidating the genetics of sex expression in the gametophyte-cosexual
(homosporous) fern Ceratopteris richardii has generated mutant
gametophytes that are all female or all male (Warne et al., 1988;
Eberle et al., 1995; Banks, 1997). Experiments examining the relative fitnesses of the different phenotypes in various combinations
of sex ratios, densities, and environmental conditions provide
opportunities to explicitly test the relative advantages of diphasy
versus dioecy, and the conditions that may select for genetically
versus environmentally determined gender.
Do gametophyte-dominant plants vary in their sporophytic
functional gender?
Where established, sex determination in bryophyte gametophytes is chromosomal, with females and males possessing a X and
Y chromosome respectively (Okada et al., 2001; McDaniel et al.,
2007; also called U and V chromosomes Bachtrog et al., 2011), segregating at sporic meiosis. As a result, the primary sex ratio in most
gender-dimorphic mosses is 1:1. However, genetic variation for differences in sex ratio does occur (Shaw and Gaughan, 1993; Shaw
and Beer, 1999; McDaniel et al., 2007). Thus the possibility exists
that there might be selection for variation in sporophytic gender.
For example, in Ceratodon purpureus, strong inbreeding depression
caused by matings between gametophytes from the same parent
sporophyte may have severe fitness effects (Taylor et al., 2007),
and in populations where spore dispersal is restricted, may result
in selection on the sex ratio. In addition, other gender dimorphic
mosses are known to abort 50% of their spores (Ramsay, 1979)
which may lead to variation in phenotypic gender of the sporophyte. In anisosporous Macromitrium weymouthii, spores exist in
four size classes, which are interpreted as females, aborted females,
males and aborted males (Ramsay, 1979).
While not documented, we can imagine the possibility of the
invasion of a gene that would preferentially abort one spore type,
resulting in sporophyte dioecy and 50% reduction in spore output.
Møgensen (1978) reported a close to 50% ratio of fertile versus
aborted spores in capsules of three moss species, and he suggested
that genetic segregation, perhaps of sex chromosomes, could be
implicated. However, in C. purpureus biased sex ratios resulting
from an interpopulation cross appear to be due to interactions
between sex chromosomes (McDaniel et al., 2007), and so other
mechanisms for sex ratio distortion are possible. If biased sex ratios
resulted in selection on sex ratios in other sporophytes in the population, then a polymorphism for all-female or all-male sporophytes
might result. While this scenario is speculative and lacking evidence, such a possibility could occur in Macromitrium, Schlotheimia
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and other gender dimorphic mosses with high numbers of spore
abortion and provide an explanation for the unexplained phenomenon termed false anisospory (Møgensen, 1978, 1983).
In species such as C. purpureus with known genetic variation for
sex ratio distortion, studies examining the response to selection
on sex ratio would provide information as to the possible constraints on sporophytic dioecy in gametophytic dominant plants.
One such constraint is the inability of sporangia on unbranched
sporophytes to specialize in male or female spore production. Thus
in bryophytes, spore abortion of one sex is likely their only route
to gender specialization. Another possible constraint is the chromosomal nature of sex determination in bryophyte gametophytes.
In polysporangiophytes, chromosomal determination of gametophyte gender appears to have been lost, and to have been replaced
by sporophytic control. Thus, in polysporangiophytes, spore gender
depends on the kind of sporangium, and gender does not segregate
at meiosis.
The challenges of applying functional gender to
non-vascular plants
Gender plasticity and labile sex expression
In many seedless plants, sex expression can change with environment, age or size, and so, for example, a small individual may
be male, but become hermaphroditic or female as it acquires more
resources (Lloyd and Bawa, 1984; Korpelainen, 1998). In these gender diphasic populations, most plants will make contributions as
both a maternal and paternal parent over its lifetime, and, if the
functional gender over the lifetime of each of the plants in the population were quantified, there would be only one gender class and
so these plants are gametophyte cosexual.
In homosporous ferns, the presence of other individuals in the
population sex as well as the age and size of the gametophyte
influence sex expression (reviewed in Cousens, 1990). In some situations, plants may reproduce over their lifetime as strictly male
or female, despite having the capacity to reproduce as either sex,
or as both (Klekowski, 1973; Atkinson, 1975). Environmentallyinfluenced sex expression is also documented in gender dimorphic
flowering plants. For example, in androdioecious Mercurialis annua
males are plastic and can become hermaphrodite at low densities (Pannell, 1997a). This type of plasticity has been considered
controversial as to whether it is true androdioecy as males are
not genetically determined (Delph and Wolf, 2005). While environmental determination will influence patterns of selection of
specialization for male and female function (as they will be completely genetically correlated) some theory about the evolution
and maintenance of dioecy should also apply in these populations (see Pannell, 2005). Regardless of the outcome of this
debate, this is not an issue solely confined to ferns or seedless
plants.
Distinguishing diphasic or labile sex expression in cosexuals
from dioecy can be problematic. Gender plots based on morphology examine only the phenotypic classes at a single point in time,
and so plots based on data from one season may not be representative of lifetime success as a female or male parent (Thomson
and Barrett, 1981). For example, plots of the gametophyte gender
of the moss Bryum lisae grown from single spores (Fig. 2a) initially reveal two discrete sex classes: plants that produce only male
sex structures (antheridia), and those that produce both male and
female (archegonia) structures. In fact, this reflects dichogamy, as
antheridia are produced before archegonia, and immature plants
are more likely to be sampled in their male phase. A reexamination
of the relative gender of plants in the greenhouse population eight
months later revealed only one phenotypic sex class (Fig. 2c; LKJ
unpubl. data).
Gender plots can also be difficult to interpret if plants exhibit
size-dependent variation in gender (as may happen in many
bryophytes and ferns) because relative measures of female and
male success are confounded with absolute investment in reproduction (Sarkissian et al., 2001). For example, if plants that are male
when small produce more male and female structures or fruit or
seeds with increasing size (e.g., Garnock-Jones, 1986; Sarkissian
et al., 2001), it would appear that large plants are more female than
small plants (see Sarkissian et al., 2001). In these situations, absolute measures of reproductive success may be more informative of
the functional role of a plant in the population.
Clonality, perenniality and infrequent sex expression
Estimates of absolute female and male reproductive success of
a gametophyte are needed to fully understand the range of sex
conditions that exist in natural populations. The paucity of this
information in non-vascular plants is likely due to the difficulty
in collecting data. Field surveys of gametophyte sex ratios are not
easily conducted in many populations due to extensive clonality
in mosses (but see Bowker et al., 2000; Stark et al., 2010), and
problems accurately identifying fern gametophytes (Hamilton and
Lloyd, 1991). In addition, extensive clonality and long genet lifespans may mean that populations may not be at an evolutionary
equilibrium (Vallejo-Marín et al., 2010).
The development of molecular markers that allow sex and
species identification and measurements of paternity and clonal
structure have recently allowed more studies of mating success
in natural populations in land plants (Korpelainen et al., 2008;
Szövényi et al., 2009; Hedenäs et al., 2010; Ricca et al., 2011). The
application of these techniques to relatively understudied species
will undoubtedly reveal a greater diversity in the sex expression
in land plants than has previously been appreciated, as well as a
greater understanding of the frequency and causes of evolutionary
transitions between breeding systems.
Acknowledgements
We dedicate this paper to the memory of David G. Lloyd
(1937–2006), teacher, mentor, and friend to us both. Our intellectual indebtedness to David should be apparent to readers. We
thank Spencer Barrett, Stuart McDaniel, and Marilyn Head and
three anonymous reviewers for comments on a previous version
of this manuscript, Monique Crawford, Lynda Delph, Sarah Eppley,
Bill Malcolm, John Pannell, and Phil Taylor for valuable discussions,
and Katie Friars and Amanda Cavanagh for assisting with moss
gametangia counts. Funding was provided by the New Zealand
Marsden Fund to P.J.G-J. and L.K.J. (grant VUW 303) and the Canadian Natural Sciences and Engineering Research Council to L.K.J.
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