Biol. Rev. (1994), 69,p p .

275-291
Printed in Great Britain

ALTERNATION OF GENERATIONS I N ALGAE: ITS

COMPLEXITY, MAINTENANCE AND EVOLUTION
BY DAVID M. JOHN
Department of Botany, The Natural History Museum, Cromwell Road,
London SW7 gBD, U K

CONTENTS
I . Introduction . . . . . . . . . . . . . . 275
11. Life History Complexity and Flexibility . . . . . . . . 276
111. Life History Types . . . . . . . . . . . . 277
( I ) Polyphasic life histories . . . . . . . . . . . 278
( a ) Two or more free-living phases . . . . . . . . 278
(b) One dependent phase . . . . . . . . . . 282
(2) Triphasic life histories in Rhodophyceae. . . . . . . . 282
IV. Evolution and Maintenance . . . . . . . . . . . 283
( I ) Florideophyte Rhodophyceae: life history patterns and zygotic amplification . 283
(2) Other life history patterns . . . . . . . . . . 284
V. Conclusions . . . . . . . . . . . . . . 287
VI. Summary . . . . . . . . . . . . . . 288
VII. References . . . . . . . . . . . . . . 288

I . INTRODUCTION
Algae are a diverse and unnatural assemblage of oxygen-producing photosynthetic
organisms. Modern biochemical, ultrastructural and, increasingly, molecular studies
have shown them to belong to several evolutionary lineages (distinct from or including
some protozoa and fungi) that arose from long-distant symbiotic events involving
plastids, mitochondria and original host cell. Evolutionary relationships remain
confused because classifications are based on characteristics of both host cell and
symbiont(s). In some classification schemes ‘algae ’ are taken to include the prokaryotic
‘blue greens’ (Cyanophyceae). Only considered here are classes of eukaryotes that
traditionally are considered to be algae (Table I ) . The focus of attention are those
classes (Chlorophyceae, Phaeophyceae, Rhodophyceae) whose study has contributed
most to our current understanding of algal life history patterns.
Life histories follow a single basic pattern in flowering plants, gymnosperms,
pteridophytes and bryophytes where a haploid gametophyte normally gives rise to a
diploid sporophyte. The term ‘alternation of generations’ is used to describe the
alternation between the two phases. It is misleading to use the term for the majority of
algae since the classical picture of a strict alternation of a haploid and diploid generation
is not always applicable. In some algae genetic and morphological alternation may not
be obligate, each generation or phase might carry on reproducing itself without
producing an alternate one. For this and other reasons, the term ‘life history’ is
preferred to ‘life cycle ’ to describe recurrent morphological and nuclear phases. A
further objection to the use of ‘alternation’ is that many algal life histories involve more
276 D. M. JOHN

than two phases. For example, red algae belonging to the Subclass Florideophycidae
(florideophyte) basically have a two-phase life history into which is inserted an
additional phase, the carposporophyte. A more appropriate term is ‘ change of
generation ’, a correct translation of the German ‘ Generationwechsel’, first used to
describe the succession of phases in the life histories of invertebrates (see Dixon, 1973,
pp. 181, 182).Further confusion has arisen through the development of a specialized
terminology for the constituent parts of algal life histories. Attempts to apply to algae
the terminology devised to describe the life histories of ‘ higher ’ cryptogams has also led
to ambiguities and misapplication of terms.
T h e review focuses on the considerable complexity and flexibility shown by those
algal life histories in which there are two or more nuclear and/or morphological phases.
Attention is drawn to the recently demonstrated existence of a considerable degree of
intraspecific variability in such life history pathways. T h e plethora of minor variations
now discovered has led Guiry & Womersley (1993) to question the practice of naming
algal life history types. Considered are current ideas concerning the evolution of algal
life histories, and experiments designed to evaluate the adaptive advantages of life
history strategies under different environmental regimes.

I1 LIFE HISTORY COJIPLEXITY A S D FLEXIBILITY

One of the major obstacles to understanding and interpreting algal life histories is a
lack of data relating to ploidy levels. Without such data it is impossible to know whether
an ‘uncoupling’ of the morphological and genetic components of a life history has taken
place. In Scytosiphon lomentaria uncoupling is considered to be partial because one
morph is haploid and the other morph either haploid or diploid. Nakamura & Tatewaki
(1975) report that the upright haploid gametangial phase of this brown alga produces
gametes that ( a ) develop parthenogenetically into an upright (identical to parent) or a
crustose morph (‘Ralfsia stage’), or (6) undergo syngamy and the zygotes give rise to
a crustose morph. Decoupling is complete in another brown alga, Petalonia, where
three morphological phases (crusts, tufts and blades) all have the same ploidy level
(Wynne, 1969). There are many similar reports of heteromorphy unlinked to changes
in ploidy level, and of isomorphic life histories where meiosis and syngamy are not
evident (see Wynne & Loiseaux, 1976). An element of doubt attaches to some reports
in the literature, especially those where the gametangial phase of a red alga develops
directly from a carpospore-derived crust. Such apomictic recycling of the gametangial
phase takes place in Mastocarpus. Maggs (1988) disagrees with Guiry & West’s ( I 984)
suggestion that populations of this red alga may be sexual, with somatic meiosis taking
place at the time of formation of the erect morph. Kuhlenkamp & Muller ( I 985) found
an unusual pathway in the brown alga Haplospora globosa. In this alga the spermatia are
non-functional and unfertilized oogonia either develop parthenogenetically into a
sporangial phase that regenerates itself by means of uninucleate spores, or produce
tetranucleate spores that germinate to give the gametangial phase. A further
complication known in brown algae is heteroblasty, a condition whereby zoids exhibit
different germination modes and develop into different morphs independent of external
conditions or sexuality (see Pedersen, I 98 I ) . Vegetative diploidization also occurs
in brown algae and involves a diploid macrothallus developing directly on a haploid
microthallus.
An unusual phenomenon observed in red algae is the production of male and female
 Alternation of generations in algae 277
reproductive organs on the tetrasporangial phase. Such ‘mixed-phase ’ reproduction is
common in one family, the Ceramiaceae, where it is believed to result from mitotic
recombination in the tetrasporophyte leading to paired islands of homozygous male and
female tissue (see Maggs, I 988). The ceramiacean alga, Aglaothamnion diaphanum, has
a phase known as a bisporophyte because it produces bisporangia rather than
tetrasporangia. On rare occasions this sporangial phase produces a functional
gametangial phase which seems to play an insignificant role in the life history. It has
been hypothesized by L’Hardy-Halos & Maggs (I 99I) that sexual reproduction in this
Aglaothamnion is becoming lost or, after speciating as a bisporophyte, the alga is in the
process of evolving sexually. By way of contrast, the bisporophytes of Aglaothamnion
byssoides are formed by mitosis of binucleate bisporangia and spermatia. It is clear from
these studies and those on brown algae (see Henry & Muller, 1983)and green algae
(Fjeld & Lovlie, 1976), that factors other than ploidy level determine whether an
individual functions as a gametangial or sporangial phase.
Deviation from alternation of a sporangial and gametangial phase in red algae, and
more ‘primitive’ brown and green algae, commonly involves a phase recycling itself. It
is possible that development of a gamete (male or female) without sexual fusion, to
produce an adult plant, might lead to the suppression of a phase and thus give rise to
a direct and single phase life history. Female gametes are more frequently reported to
undergo parthenogenesis than male gametes. Such a difference in frequency might
account for the increase in female to male ratios of gametangial phases in populations
of brown algae where sexual reproduction is infrequent (e.g. Cutleria cylindrica, see
Kitayama et al., I 992). Apomictic reproductive structures are often morphologically
indistinguishable from those produced in sexual life histories. Doubt thus attaches to
some earlier reports of apomixis where no information is given on chromosome
numbers. Data on apomixis still remains meagre, but what reliable evidence is available
suggests that few species are ‘obligate ’ apomicts (all populations reproducing
completely asexually). An advantage of apomixis is that it enables a morph to survive
in a particular environment, whereas sexual reproduction might result in one that is an
inappropriate morph because it would be at a selective disadvantage. Apomixis might
be expected to be more important in severely disturbed habitats where selective
pressures differentially act against one type of morph compared to another. Vegetative
propagation and apomixis should be more frequent in ecologically-marginal environ-
ments (e.g. close to the distributional limit of a species) where a single spore or
propagule might be expected to develop into a founder individual.
What is becoming increasingly apparent is that : ( a ) research on life history pathways
needs to be conducted throughout the range of an alga and under different environ-
mental conditions, ( b ) further investigation is required of the role played by asexual
reproduction in life histories, ( c ) karyological investigations are essential, as morpho-
logically indistinguishable reproductive structures may have different chromosome
numbers, and uncoupling of morphological and nuclear phases is common in algae, and
( d ) a priority area for future research is the study of genetic and environmental control
of algal life histories.

111. LIFE HISTORY TYPES

The life histories of the different algal classes have much in common, with the
exception of the triphasic type found in a red algal subclass, the Florideophycidae. For
278 D. M. JOHN

the large majority of algae details of their life histories remain unknown, meagre or
equivocal. Only in three classes (Chlorophyceae, Phaeophyceae, Rhodophyceae) is the
available information sufficiently comprehensive and reliable to allow meaningful
generalizations to be made. Many earlier generalizations have had to be modified or
discounted due to new information, doubt attaching to the evidence, or a failure in the
past to evaluate critically all the information. A particular problem has been a lack of
appreciation that algae are capable of exhibiting considerable intraspecific variation in
their life history patterns (for review of red algae, see Maggs, 1988).
T h e three basic life history types recognized in algae are linked to differences in the
degree of morphological elaboration of the phases. One type has a single free-living
haploid or diploid phase, and the other two types possess more than one phase. T h e
former type occurs in the morphologically more advanced orders of brown algae, the
Fucales, Ascoseirales and Durvilleales. In these orders the single phase is diploid and
produces by meiosis haploid gametes (diplontic life history). Only a small minority of
algae have a single haploid phase with meiosis taking place on germination of the
zygote. Such a haplontic life history is reported in a few macroscopic members of one
brown algal order, the Fucales, and some orders of green algae (e.g. Charales,
Charophyceae). Evidence from various sources indicate that the Charophycean genus
Coleochaete exhibits traits in common with what might be considered to be the
immediate ancestors of embryophytic plants (see Graham, 1985; Graham et al., 1991).
T h e ‘direct type’ or monophasic life history found in most algal classes (Table I ) is
usually regarded as the most primitive. It is not considered further here except when
closely linked to biphasic or polyphasic life histories.

(I) Polyphasic life histories

( a ) Two or more free-living phases
Sporic life histories typically consist of a spore-producing phase (usually diploid)
alternating with a gamete-producing phase (usually haploid). Such an alternation of
two nuclear phases is a biphasic or diplohaplontic type of life history. T h e
morphological phases linked to the nuclear phases are either isomorphic (e.g.
Chlorophyceae : Ulvales [except Family Monostromataceae], Cladophorales ; Phaeo-
phyceae : Ectocarpales, Tilopteridales, Sphacelariales, Dictyotales) or heteromorphic
(e.g. Chlorophyceae : Acrosiphoniales, Derbesiales ; Phaeophyceae : Chordariales,
Dictyosiphonales, Sporochnales, Desmarestiales, Laminariales, Scytosiphonales ; Rho-
dophyceae : Bangiales). T h e diploid phase either produces haploid spores by meiosis
(hence meiosis is sporic), or diploid spores that on germination undergo meiosis (e.g.
conchospores of Porphyra). Alternatively, its somatic cells undergo meiosis and give
rise directly to the haploid phase. T h e haploid phase might be monoecious or dioecious
and generally produces gametes by mitosis. In some cases different morphs possess the
same chromosome complement (pleiomorphy) resulting in a single nuclear phase and
two or more morphological phases.
A diplohaplontic life history of an alternation of morphologically identical haploid
and diploid plants (isomorphic life history) is the commonest type. Uncertainty
frequently surrounds the extent to which the morphologically identical phases are
physiologically and ecologically equivalent. Various observations on brown algae (see
 Alternation of generations in algae 279
Table I. The distribution of single or two or mure phase life histories in the classes of
eukaryotic algae
Single phase : Two phases :
somatic cells different and/or
diploid or haploid same ploidy level
Kingdom Plantae'
Subkingdom Viridiplantae
Chlorophyta2 (Green Algae)
Chlorophyceae + +
Prasinophyceae + -
Ulvophyceae + +
Charophyceae +
Subkingdom Biliphyta
Rhodophyceae (Red Algae) +
Glaucophycocystophyceae +
Kingdom Chromista
Chromophyta sensu lato
Bacillariophyceae +
Chrysophyceae +
Cryptophyceae +
Eustigmatophyceae +
Phaeophyceae ( = Fucophyceae, Brown Algae) +
Prymnesiophyceae ( = Haptophyceae) +
Raphidophyceae +
Synurophyceae +
Xanthophyceae ( = Tribophyceae) +
Kingdom Protozoal
Euglenophyceae +
Dinophyceae +
' Classification into kingdoms follows Cavalier-Smith (1981, 1983).
Classification mainly follows the class-level system for Chlorophyta proposed by Mattox & Stewart (1984).

Clayton, 1988) suggest that the sporangial phase is better able to survive a wider range
of conditions than the gametangial phase. In many brown algae (e.g. Ectocarpus,
Dictyota) and green algae (e.g. UZva) the haploid phase is monoecious. If the haploid
plant is dioecious then male and female plants are frequently morphologically
indistinguishable. One member of the red algal order Palmariales, Palmaria, has a
tetrasporangial phase which closely resembles the male gametangial phase (see Van der
Meer & Todd, 1980). In Palmaria the tetrasporangial phase is large and its holdfast
completely overgrows the microscopic female plant (see Fig. I G). If dissimilar to the
male gametangial phase then the tetrasporangial phase is either just two cells (stalk cell
and tetrasporocyte) or a system of filaments spreading over the female gametangial
phase. The order therefore has an unusual alternation of isomorphic (albeit
tetrasporangial phase and male plant only) and heteromorphic phases.
The sporangial phase is dominant in four algal classes (see Table I ) possessing
heteromorphic life histories. In some orders of brown algae (e.g. Laminariales,
Dictyosiphonales, Desmarestiales, Sporochnales, Syringodermatales) the sporangial
phase is diploid, relatively large, often long-lived and regularly alternates with a
diminutive, short-lived, haploid phase. Only in a few brown algal genera (e.g. Cutleria,
Scytosiphon, Petalonia) is the haploid phase dominant (see Table 2). Biphasic
280 D. M. JOHN

Fig. I.Examples of life history diversity in the Khodophyceae. Symbols: s , position of syngamy; m,
position of meiosis; n, haploid; zn, diploid (Figs A, B, D, E and G are after Dixon, 1982).

heteromorphic life histories are known in some genera of green algae (e.g. Ulothrix,
Acrosiphonia, Monostroma) and red algae belonging to the order Bangiales (e.g. Bangia,
Porphyra, Porphyropsis, Smithora). Various interpretations have been placed on life
history patterns in the Bangiales and these revolve around whether the post-fertilization
products represent a carposporangial phase or not. I n the present review the order is
accepted as having a biphasic, rather than a triphasic life history (for discussion, see
Hawkes, 1992).
T h e different phases of some algae are morphologically so dissimilar that until
recently they were considered to be different species or genera (Table 2) and, in a few
cases, genera were placed in separate families or orders. I t is still common practice to
refer to the less conspicuous phase/stage by the generic name it was once given (e.g.
Conchocelis-phase, Chantransia-stage, Falkenbergia-stage, Codiolum-phase), or to a
genus it resembles (e.g. Audouiniella-like, Ralfsia-like, Myrionema-like, Compsonema-
like). Heteromorphic life histories occur in the Prymnesiophyceae (see Table I ) , but
many of the details remain obscure. For example, in Phaeocystis pouchetii there is no
information on the chromosome number of its colonial and flagellated morph (see
Sournia, 1988). I n other algal classes it has been established unequivocally that
different morphs exist with identical chromosome numbers and no evidence of
sexuality. For example, many brown algae in the orders Chordariales and Dictyo-
siphonales possess an asexual, heteromorphic life history termed ' direct ' and
monophasic (see Fletcher, 1987).
 Alternation of generations in algae 28 I

Table 2 . Examples of heteromorphy in taxa belonging to three major classes where

biosystematic studies have elucidated many details of their life history
(A) Two morphological phases: haploid gametophyte and diploid sporophyte
Chlorophyceae
Gametangial phase Sporangial phase Reference(s)
Acrosiphonia ‘ Codiolum/Chlorochytrium’ See Tanner, 1981
Caposiphon
Monostroma
Ulothrix
Bryopsis ‘ Derbesia ’ Rietema, 1975
Halicystis
Phaeophyceae
Sporangial phase Gametangial phase Reference(s)
Laminariales : Minute, filamentous See Wynne & Loiseaux, 1976
Laminaria
Saccorhiza
Sporochnales
Desmarestiales
Gametangial phase Sporangial phase Reference(s)
Scytosiphon ‘ Ralfsia’ See Wynne & Loiseaux, 1976
Petalonia
Cutleria ‘ Aglaozonia ’
Rhodophyceae
Sporangial phase Gametangial phase Reference(s)
Porphyra, ‘ Conchocelis’ Drew, 1949
Bangia
Lemanea, ‘ Chantransia’ Magne, 1969
Batrachospermum
Thorea
(B) Three morphological phases (florideophyte Rhodophyceae) : free-living haploid gametangial phase,
dependent diploid carposporangial phase, free-living tetrasporangial phase
Gametangial phase Sporangial phase Reference(s)
Acrosymphyton ‘ Hymenoclonium ’ Cortel-Breeman & Hoek, 1970
Ahnjeltia ‘ Porphyrodiscus’ Farnham & Fletcher, 1976
Asparagopsis ‘ Falkenbergia’ Feldmann & Feldmann, 1942
Bonnemaisonia ‘ Trailliella’ Feldmann & Mazoyer, 1937
Gymnogongrus ‘ Erythrodermis-Petrocelis ’ Hollenberg, 1943; DeCew &West, 1981
Halarachnion ‘ Cruoria’ Maggs & Guiry, 1987, 1989
Turnerella ‘ Cruoria’ South et al., 1972; Maggs & Guiry, 1989
Opuntiella ‘ Cruoria’ DeCew et al., 1992
Mastocarpus ‘ Petrocelis’ Guiry et al., 1984; West, 1972; West et al., 1977
Phyllophora ‘ Erythrodermis’ M a w , 1989
Schizymenia ‘ Haematocelis’ Ardre, 1977
Sphaerococcus ‘ Haematocelis’ Maggs & Guiry, 1982
Farlowia ‘ Haematocelis-Cruoriopsis ’ DeCew & West, 1982
Gloiosiphonia ‘ Cruoriopsis ’ DeCew et al., 1982; Edelstein, 1970, 1972; Edelstein &
McLachlan, 1971
282 D. M. JOHN

( h ) One dependent phase

This covers life histories in which the two phases are in intimate association. For
example, in the green algae Prasiola meridionalis and P. stipitata the free-living phase
is diploid and monostromatic. T h e gametangial phase develops on it by some cells
undergoing meiosis to form paired male and female areas of polystromatic tissue
(Friedman, 1959). These areas of gametangial tissue produce gametes by mitosis and
syngamy gives rise to a zygote that germinates into the free-living diploid phase. Other
species of Prasiola have both heteromorphic and zygotic life histories.
A single phase life history pattern is reported in the red alga Helminthocladia
senegalensis (Bodard, I 97 I ) . It is assumed that the haploid carpotetraspores produced
by the carposporangial phase give rise to the gametangial phase (Fig. I E ) . Doubt
attaches to the existence of such a life history and further culture-based research is
needed. Another variant occurs in the red algal family Phyllophoraceae (e.g.
Gymnogongrus, Phyllophora) where a spreading mass of tissue, the tetrasporoblast,
grows over the surface of the gametangial phase and produces spores by meiosis (Fig.
I F).

(2) Triphasic life histories in Rhodophyceae

Three phase life histories occur in all orders of the red algal subclass Florideo-
phycidae, with the exception of the Palmariales. Typically the life history consists of a
gametangial phase and two morphologically-distinct spore-producing phases, the
tetrasporangial (tetrasporophyte) and carposporangial (carposporophyte) phase. T h e
latter differs markedly in appearance from the female gametangial phase on which it
develops. It is a dependent phase superimposed on what otherwise is basically a
biphasic life history. Mitotically-produced spores on the carposporangial phase give
rise to the sporangial phase which usually produces tetrasporangia or, much less
commonly, bisporangia or polysporangia. T h e sporangial phase has a free-living
existence or develops on the female gametangial phase (see Fig. I F).
T h e most typical life history pattern involves two free-living phases, the gametangial
and the tetrasporangial, and a dependent carposporangial phase. In red algae, life
histories with isomorphic free-living phases (Fig. I A, Polysiphonia-type) are more
common than those with heteromorphic phases. Nonetheless, culture-based research is
continuing to add to the numbers of algae known to have heteromorphic life histories
(see Table 2 ) . T h e gametangial phase is usually more conspicuous (Fig. I D) than the
tetrasporangial phase which is often in the form of a crust (e.g. Mastocarpus, West
et al., I 977), or tufts of branched filaments (e.g. Liagora spp., see Guiry, 1990; Brodie &
Norris, 1992; Asparagopsis, Feldmann & Feldmann, 1939). Only in one red algal order,
the Acrochaetiales, is the tetrasporangial phase more conspicuous than the gametangial
phase (Fig. I C ) . If the carposporangial phase is considered as equivalent to other life
history phases then all red algae possessing it are heteromorphic.
A variant of the triphasic life history pattern is found in such freshwater genera as
Batrachospermum, Lemanea and Thorea. In these algae a tetrasporangial stage is absent
but instead the diploid carpospores germinate to form a filamentous ‘juvenile’ phase.
Apical cells of the juvenile phase undergo meiosis and these haploid cells develop in situ
to form the gametangial phase (Fig. I D). Further research is required to verify and
fully establish details of this life history type.
 Alternation of generations in algae 283
IV. EVOLUTION AND MAINTENANCE OF LIFE HISTORIES
Life history patterns can be interpreted as adaptive strategies whose characteristics
have evolved in response to various selective pressures. In that they play a role in
determining the biological fitness of a species they are of special evolutionary
importance. The bewildering variety of growth forms and life history patterns in algae
is considered a reflection of the diversity and complexity of the selective agencies
operating in aquatic environments. Unfortunately knowledge of the life histories of the
majority of algae remains meagre or non-existent, with intraspecific variation only taken
into account in few recent studies. As a consequence the evolutionary and functional
significance of generation change are still little understood.

(I)Florideophyte Rhodophyceae :life history patterns and zygotic amplification

Much of the debate concerning the evolution of algal life histories centres on the red
algae, a class exhibiting an extraordinary degree of life history complexity. One of the
early postulates considered the commonest type of life history in florideophyte red
algae, the Polysiphonia-type, to represent the ancestral pattern (see Feldmann, 19-72;
Magne, 1972).It has been pointed out by Guiry (1987)that certain ‘advanced’ red algal
orders (Rhodymeniales, Ceramiales) also possess the Polysiphonia-type. In contrast,
numerous members of so-called ‘ primitive ’ orders (e.g. Acrochaetiales, Nemaliales)
have a type (Bonnemaisonia hamifera-type) that is considered to have been derived from
it. In view of these observations it has been conjectured that red algal life histories have
evolved independently. Cladistic analysis by Gabrielson & Garbary (I 986) supported
the view that red algal life history patterns have evolved on several occasions in different
phylogenetic lineages, so making it unclear as to which to regard as the more primitive.
Maggs (I 988)considers it a mistake to place too much phylogenetic significance on life
history patterns in red algae in view of the high degree of interspecific and intraspecific
variation displayed by them.
Many freshwater red algae have a unique life history pattern in which only one type
of spore is produced, the carpospore. This spore gives rise to a microscopic phase which
in turn produces the erect gametangial phase following meiosis of the apical cell (see Fig.
I D). Such a life history type is considered to be an adaptation for growth in rivers and
streams where water flow is unidirectional (see Sheath, 1984; Sheath & Hambrook,
1990). It enables the perennial microscopic phase to maintain its upstream position
while the larger upright phase is produced seasonally. T h e alga, therefore, continues to
proliferate from the microscope phase and the released spores enable downstream
colonization to take place. If flowing-water algae possessed a life history involving just
spore release then a population would be unable to maintain its position and so
gradually shift downriver.
Searles (I 980)postulated that the carposporangial phase evolved in situ as a means of
achieving ‘zygotic amplification ’. Amplification enables a many fold increase in the
numbers of nuclei resulting from a single fertilization event and compensates for the
relative infrequency of syngamy. Infrequency of syngamy in red algae is due to the non-
motility of the spermatia and hence their passive transfer to the carpogonia. The need
for efficient dispersal is considered to be a significant factor in the evolution of the
carposporangial phase (see Hawkes, I 990). Two hypothetical methods of achieving
zygotic amplification have been proposed : (a) formation of a free-living tetrasporangial
14 B R E 69
284 D. M. JOHN
phase direct from the zygote, with the spores produced giving rise to the gametangial
phase (biphasic life history), and (b) formation of a mitosporangial or carposporophyte
phase, with or without the spores giving rise to a free-living tetrasporangial phase
(triphasic life history). Amplification is achieved by the carposporophyte generation
producing large numbers of dispersible products (carpospores) from a single
fertilization event (Fig. 2). Wilce & Searles (1991) have estimated that in Schmitzia
sanctae-crucis each zygotic nucleus divides perhaps 4500-fOld in producing carpospores.
It has been hypothesized that such amplification might have evolved several times in
red algae possessing a Polysiphonia-type of life history, and independently in the
Acrochaetiales or primitive members of the Palmariales. According to Searles (1980),
in evolutionary terms the production of a carposporangial phase is more successful than
direct development of a tetrasporangial phase from the zygote. Its advantage is in
maximizing potential recombination and genetic diversity resulting from a single
fertilization event. Searles considers the primitive ancestral condition to be sexual, with
only the gametangial and tetrasporangial phase present. Red algae with biphasic life
histories have single-celled carpogonia and terminally-formed tetrasporangia that are
cruciately cleaved (Guiry & Womersley, 1993).

(2) Other life history patterns

Scagel et al. (1982) postulated an evolutionary sequence for the main types of
alternation of generations. They considered gametic and sporic meiosis types in algae
to have evolved from zygotic meiosis, the former resulting in diploid organisms and the
latter in an alternation of generations. It is suggested that evolution proceeded to
isomorphic and heteromorphic types, but it was diploid-dominant algae that gave rise
to terrestrial plants. T h e migration to land thus resulted in the survival of only one life
history type and eliminated much of the potential for flexibility. In the major algal
classes isomorphic and heteromorphic types are widespread and opinions differ as to
which to consider the more primitive. In brown algae Clayton ( I 988) regards both types
to have probably existed as long as the class.
Research on the adaptive features of different life history morphs has tended to focus
on heteromorphic life histories. lstock ( I 967) suggested that selection acting
independently on different morphs is likely to result in the eventual elimination of one,
or to reduce it in favour of the other. If selection acts in this way then heteromorphic
life histories would be expected to be inherently less stable than isomorphic ones, and
yet there is no evidence to suggest this to be the case. A wide variety of agencies are
likely to play a role in the evolution and maintenance of heteromorphic life histories.
Selective agents might be abiotic, as demonstrated in studies of algae growing on
unstable hard substrata (e.g. cobbles formed of calcareous red algae) where seasonal
instability has been correlated with the custose habit and/or the life history strategy (see
Lieberman et al., 1984). The crustose phase of the brown alga Scytosiphon lomentaria
is considered by Littler & Littler (1983) to be a morph well-adapted to survive harsh
winter conditions and to resist seasonal sand-scour, burial and wave-shear. In southern
Australia the crustose morph over-summers because it is capable of surviving intense
insolation and high air temperatures. Experimental studies have demonstrated that in
some environments herbivore grazing is the principal agent responsible for morph
 Alternation of generations in algae
Syngamy
I
Zygote dispersed Only one
3 diploid spore dispersed
L Zygote undergoes
3 single mitotic
(e.g. Rhodochaete)
Zygote or its division Meiosis produces
derivative four haploid spores
undergoes in dispersed
situ development (e.g. Rhodophyserna)
on haploid
gametophyte
\
Zygote or its
derivative
undergoes many
mitotic divisions

-
J L Diploid phase
Diploid phase
borne on haploid independent,
meiosporangial

Several
i L
Single Meiosporangial
*
Meiosporangial
mitosporangial mitosporangial phase borne on phase overgrows
phases from single phase from single haploid diminutive
fertilization; fertilization; gametophyte, haploid female
many diploid many diploid diminutive; gametophyte;
spores dispersed spores dispersed many haploid many haploid
(e.g. Schmitzia) (e.g. Ceramiales) spores spores
dispersed dispersed
(e.g. Liagora (e.g. Palmaria)
tetrasporifera)

Fig. 2 . Some of the main trends in rhodophyte sexual reproduction indicating amplification of products
from a single fertilization (modified after Hawkes, 1990).

selection and leads to convergence of life history patterns. For example, Lubchenco &
Cubit ( I 980) demonstrated that the mortality of different life history morphs of certain
intertidal algae was controlled by herbivore grazing. Fleshy upright morphs were found
to be selectively removed by seasonally-intense grazing whereas crustose or substrate-
boring morphs were resistant to grazing. Under light grazing pressure the upright
morphs were competitively superior to the alternate phase because of their faster
establishment on surfaces, more rapid growth rate and earlier reproductive maturity.
The spreading of different sources of mortality over different morphs in heteromorphic
life histories was termed ‘bet-hedging’ by Slocum (1980).
Water motion is an important selective agency and, when severe, prevents the
development of all morphs with the exception of crustose, low mat or cushion-like
forms and larger upright ones possessing exceptionally tough and pliable thalli. Severe
wave-crash and drag tends to result in the dominance on wave-exposed rocky shores of
low growing forms, and upright alternative phase(s) tend to be absent unless wave
action is itself seasonal. In freshwater environments hydraulic resistance to flow is
considered more important than grazing and desiccation as a major environmental
pressure leading to the evolution of a ‘bet-hedging’ or ‘two-edged’ life history strategy
in red algae. Freshwater reds frequently grow in running-water and many have an
upright macroscopic phase and a much less conspicuous creeping or prostrate phase.
The macroscopic gametangial phase is often relatively fast-growing and is subject to a
14-1
 D. M. JOHN

Table 3. Predictions of Lubchencko W Cubit (1980) as to the predominant life histories t o

be found in ephemeral shore algae under different grazing regimes
(Grazing \ \ a s defined as the probability that a given individual will be removed b y herbivory in a given
interval of time. ‘Variable’ is taken to mean that grazing fluctuates m-ith periods of high and low pressure,
exceeding the generation times of crustose/boring and upright morphs, respectively. Predictable grazing is
when it can he forecast, this often correlates with time or another environmental cue.)
Grazing Prediction

flLight 4 Isomorphy, competitively superior

Constant upright morphs predominate

%kHeavy 4 Isomorphy, grazer-resistant crustose boring

morphs predominate

4 Predictable > Heterornorphy, alternation of production

and predominance of morphs
Yariable

%Unpredictable > Heterornorphy, continuous production

(but not s u n i v a l ) of both morphs

considerable degree of pull, battering and abrasion during flood periods. I n contrast,
the slower growing prostrate phase avoids hydraulic stress by living within the
boundary layer, but is likely to suffer lack of nutrient replenishment and is vulnerable
to increased grazing and competition from other benthic organisms. I n temperate
regions, the minute sporangial phase (so-called Chantransia phase) of such freshwater
red algae as Lemanea and Batrachospermum is perennial. T h e sporangial phase is usually
most evident over the winter period when violent floods frequently lead to the removal
of the larger gametangial phase. Exposure t o air during summer lowering of water levels
often leads to desiccation. I n Lemanea the perennial sporangial phase has been found
to be more tolerant to drying than the gametangial phase (Everitt & Burkholder, 1 9 9 1 ) .
Another red alga, Thorea, can persist as its microscopic sporangial phase and several
years may elapse before the more conspicuous gametangial phase is produced (see John
et al., 1989). T h e r e is evidence to show that in freshwater red algae the alternation of
phases is influenced by latitude, timing of tree canopy development, and seasonal
changes in photoperiod and temperature (see Sheath, 1984, p. 142). Seasonal
perturbations in temperature, water levels, light penetration, depth and turbidity are all
factors that have been suggested as accounting for the high proportion of freshwater red
algae having heteromorphic life histories.
Algae having heteromorphic life histories are considered to be at an adaptive
advantage if the principal selective agent(s) is variable rather than constant. If variable
then the environment may be regarded as divided into alternate niches, or partitioned
into different niches thus resulting in a complex habitat mosaic (e.g. a patchwork of
intensely and less intensely grazed areas). T h e adaptive advantage or disadvantage of
different life history types depends on environmental partitioning and the selective
agencies operating on them. Lubchenko & Cubit (1980) carried out an investigation of
ephemeral algae on shores in New England and were able to predict what would be the
predominant life history under different environmental and grazing regimes (Table 3).
If grazing was constant they predicted that algae having an ‘obligate’ alternation of
different free-living morphs would be at a selective disadvantage due to competition
eliminating one morph. Should an alga have different life history phases then a single
 Alternation of generations in algae 287
phase would survive, but reproductive effort is wasted if production continues of the
morph(s) that would be eliminated by selection. Isomorphy was regarded as
advantageous under relatively constant conditions and heteromorphy advantageous
under predictable or unpredictable grazing pressure, especially if there was continuous
production of both morphs. It seems that greater fitness accrues to those algae which
allocate resources to synchronizing the production of the morph which is most likely to
survive (e.g. grazing-resistant morphs during season of intense herbivory). For
synchronization to evolve, the selective agent(s) must be predictable and the appropriate
morph produced in response to environmental cues. In Lubchenko & Cubit’s (1980)
study the environmental cues were photoperiod and temperature, or both acting
toget her.
Theoretical studies of life history models have concluded that seasonality is crucial
in the evolution of life histories where there is more than one ecologically distinct phase
(Istock, 1966). The converse is expected to be true, with direct or isomorphic life
histories at a selective advantage in constant or stable environments. Some tropical
environments are relatively stable (e.g. coral reef systems) and it may be speculated that
in such environments selection would favour a single morph as different ones would
confer little ecological advantage. In support Clayton (1987) cites the frequent
occurrence in the tropics of brown dictyotalean algae in which life histories are
isomorphic. She points out that brown algae having heteromorphic life histories are
poorly represented in the tropics and yet dominate in temperate and polar seas. Studies
of algal floras on coral reefs tends to centre on the structural and biochemical strategies
that allow survival of intense grazing pressure rather than on life histories.
It has been speculated that the direct life history type (single morph) might be
derived from a heteromorphic type and three possible mechanisms have been proposed
(see Maggs, 1988, 1989). In cultures of the red alga Mastocarpus, the failure of the
direct type of life history (female gametangial phase) to revert spontaneously to a sexual
type has led Maggs ( I 988) to suggest that populations having different life histories may
be genetically isolated. Until this is investigated experimentally, it is only possible to
speculate on the adaptive advantages of monophasic life histories and those in which
there are two morphologically identical phases.

V. CONCLUSIONS
Our current understanding of algal life histories owes much to culture-based research
carried out over the past two decades. Nonetheless, only a small percentage of algae
have yet been examined and attention has tended to focus on macroscopic seaweeds
rather than on microscopic forms. Much of the information on life histories is
descriptive, with virtually nothing known of regulatory mechanisms and their degree of
stability. Karyological information is lacking in many studies and yet without
knowledge of ploidy levels it is impossible to interpret life history events. What is
required are further descriptive accounts of life history patterns in a greater range of
algae than studied hitherto, more karyological investigations, and linked field/laboratory
studies on interaction between algal life histories and environmental influences.
Knowledge of environmental control is essential to our understanding of not only
algal distribution patterns but inter- and intraspecific life history variation. What is
also needed is the further development of De Wreede & Klinger’s (1988) attempt to
288 D. M. JOHN

incorporate knowledge of algal life histories into life history theory and to explore it in
terms of evolutionary processes.
VI. SUMMARY
Life histories of photosynthetic eukaryotes traditionally-termed algae exhibit a
considerably greater degree of complexity than those of ' higher cryptogams.' Some
algae have a so-called ' obligate ' alternation between spore-producing and gamete-
producing phases, but the majority seem capable of following other pathways depending
upon environmental conditions. In only four algal classes do life histories show a change
in morphological and/or nuclear phases. The following basic life histories are
recognized in the Chlorophyceae, Phaeophyceae and Rhodophyceae : ( a ) monophasic,
a diploid or haploid phase, ( b ) two or more phases, most commonly an alternation of an
isomorphic or heteromorphic haploid gametangial phase and a diploid sporangial
phase, and (c) three phases (unique to florideophyte Rhodophyceae), with a diploid
spore-producing phase (carposporophyte) developing on the gametangial phase, a
diploid phase (tetrasporophyte if meiosis is sporic) and a haploid gametangial phase.
Evidence from recent research indicates that in many algae there is an uncoupling of the
morphological and nuclear phases. The dominance of one phase and suppression of
another has been suggested to be due to the common occurrence in algae of apogamy,
apomeiosis and parthenogenesis. Free-living morphs in heteromorphic life histories
may be morphologically so dissimilar that formerly they were attributed to different
genera.
Evolution of the carposporangial phase in red algae is speculated to be a means of
achieving zygotic amplification to compensate for the infrequency of syngamy. Such
amplification allows the production of a large number of dispersible products from a
single fertilization. The direct development of a free-living tetrasporangial phase is
considered another mechanism for achieving amplification. In freshwater red algae the
growth of an upright phase from a perennial microscopic one is considered an
adaptation for maintaining their upstream position.
Life history pathways in algae are controlled by subtle environmental influences (e.g.
photoperiodism, temperature, light quality, nutrients). Experimental evidence is
lacking to support the contention that spatial and/or temporal partitioning of the
environment is a mechanism favouring the maintenance of heteromorphy. Herbivory
is known to be an important selective force suppressing some morphs and accentuating
the seasonal dominance of others. Differential resistance of morphs to herbivory
in environments where grazing intensity is predictable may lead to the selective
maintenance of heteromorphy.
Algal life history patterns are unexplored in terms of evolutionary processes. Various
models for the evolution of biphasic or polyphasic life histories stress the importance
of the capacity for both asexual dispersal of successful genotypes and for the generation
of new genotypes via meiosis and syngamy. All evidence points to the fact that many
life history processes operative in algae differ significantly from those described for
other cryptogams.
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