Biological Journal of the Linnean Socieg (1986), 28: 321-329. With 1 figure
Automixis: its distribution and status
MICHAEL MOGIE
School of Biological Sciences, University of Bath, Claverton Down, Bath BA2 7AT
Accepted for publication I0 February 1986
Biologists have conclusively failed to arrive at a generally acceptable definition of sexual
reproduction. Because of this, several reproductive processes are seen as sexual by some authors but
as asexual by others. Included among these are automictic methods of reproduction. Automixis
describes several reproductive processes whereby a new individual derives from a product or
products of a single meiotically dividing cell. Several forms involve an episode of nuclear fusion and
it is argued that, because of this, they should be seen as sexual processes irrespective of whether the
fusing bodies are differentiated as gametes or are simply meiotic tetrad nuclei. Other forms involve
no episode of nuclear fusion and it is argued that, because of this, they should be seen as asexual
processes. These latter forms involve the generation of diploid eggs either by restitutional meioses,
or by an endomitotic event preceding or following a reductional meiosis, or involve the generation
of a diploid embryo by the fusion of cleavage division nuclei in a haploid embryo; in each case the
egg develops parthenogenetically.
In addition to the disagreement that exists over the reproductive status of automixis, considerable
confusion exists over its taxonomic distribution. It is often described as being restricted to a few
species of insects, where it is parthenogenetic, but in fact it occurs across a wide range of taxa,
including both isogamous and anisogamous plants and fungi, where it may be either
parthenogenetic or non-parthenogenetic. This confusion results both from a failure of many
biologists writing on this subject to adequately consider the variation in life-cycles existing between
major taxa and from a general failure by botanists and mycologists to distinguish between
automixis and autogamous forms of self-fertilization (in which the fusing nuclei derive from
different meioses). It is further compounded by a proliferation of synonyms for automictic processes.
Thus in a number of publications automictic processes are variously described as being
matromorphic, thelytokous, parthenogamic, autogamic or apomictic rather than as being
automictic.
KEY WORDS:-Sexual
reproduction - asexual reproduction
-
parthenogenesis
-
automixis.
CONTENTS
Introduction . . . . . . . .
. . . .
Definitions and descriptions
Automixis as a sexual or an asexual process.
References. . . . . . . . .
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
321
322
327
329
INTRODUCTION
The advantages and disadvantages of sexual and asexual methods of
reproduction have been vigorously debated in recent years (e.g. Williams, 1975;
Maynard Smith, 1978; Bell, 1982). Surprisingly, this debate has progressed in
the absence of any generally accepted definition of what processes or events
32 1
0024-4066/86/070321+ 09 $03.00/0
0 1986 The Linnean Society of London
322
M. MOGIE
comprise sexual reproduction. Indeed, many of the numerous definitions
proffered by the literature are incompatible, a situation which has resulted in
several reproductive processes being considered sexual by some authors but
asexual by others. Prominent among these are automictic methods of
reproduction (see Table 1 and references therein). Automixis will be defined
fully in the next section; briefly, it comprises processes whereby a new individual
derives from a product or products of a single meiotically dividing cell. A
comparison of the different types of definition of sexual reproduction prevalent
in the literature will be made later, when the status of automixis as a sexual or
an asexual process is discussed.
In addition to the confusion existing over its sexual or asexual status,
considerable confusion also exists both over the taxonomic distribution of
automixis and over its status as a parthenogenetic or non-parthenogenetic
process (parthenogenesis involves the development of a new individual from an
unfertilized egg). For example, automixis has been described as being restricted
to a few parthenogenetic animal species (Maynard Smith, 1978); however, it
also occurs among flowering plants, where it is parthenogenetic, and among
lower plants and fungi, where it is often non-parthenogenetic. These underestimations result from a lack of consideration of differences in life-cycles between
major taxa and from a failure to appreciate that automictic process in plants
and fungi are described as matromorphic (Asker, 1980), autogamic (Drebes,
1977), apomictic (Klekowski, 1973) or as instances of self-fertilization (Fincham,
1983) rather than as automictic. The term ‘automixis’ is largely restricted to the
zoological literature although even here synonyms have been used (see Table 1).
These points are discussed in the following section.
DEFINITIONS AND DESCRIPTIONS
Reproductive processes that involve an egg cell
Most reproductive processes involve a nuclear fusion-meiosis cycle. These can
be classified using the ancestry of the fusing nuclei. If the nuclei are derived
from different zygotes then the process is one of allogamy. If they are derived
from the same zygote then the process is either autogamous or automictic. With
autogamy the fusing nuclei are products of different meioses. With automixis
they are products of the same meiosis. The nuclei which fuse in automictic
reproduction may comprise any two of the four meiotic tetrad nuclei or their
mitotic derivatives, or any two nuclei derived mitotically from a single tetrad
nucleus. The genetic consequences of allogamy and autogamy are well
documented (e.g. Falconer, 1981). Those for automixis have been described by
White (1973) and Maynard Smith (1978) and will only be mentioned briefly
here. If the nuclei which fuse are copies of a single tetrad nucleus then the
progeny will be homozygous at all loci. If they are two of the tetrad nuclei or
their derivatives then the levels of homozygosity in the progeny will be greater
than that in the parent, with the identities of the nuclei being important in
determining which loci are likely to become homozygous. Thus during the first
meiotic division the egg mother cell gives rise to two nuclei (A and B) each of
which gives rise to two derivatives (a,a and b,b) during the second meiotic
division. If sister nuclei fuse (Le. a x a or b x b) homozygosity may increase
automixis/asexual
automixis/asexual
automixis/asexual
automixis/sexual
matromorphy/asexual
thelytoky/asexual
(not described)
(not described)
(not described)
(not described)
automixis/asexual
automixis/asexual
automixis/asexual
automixis/sexual
(not described)
parthenogamy/asexual
(not described)
automixis/sexual
autogamylsexual
(not described)
(not described)
(not described)
(not described)
(pre-)thelytokous/asexual
(post-)automixis/asexual
automixis/asexual
(not described)
automixis/sexual
matromorphy/asexual
thelytoky/asexual
(pre- apomixis/asexual
Diploidy restored by the
Diploidy restored
fusion of cleavage division following pre- or postnuclei (P)
meiotic endomitosis (P)
Diploidy restored by the
fusion of meiotic tetrad
nuclei (P)
(not described)
(not described)
(not described)
automixis/asexual
apomixis/asexual
automixis/sexual
matromorphy/asexual
thelytoky/asexual
(not described)
automixis/asexual
Diploidy achieved by
automictic restitution (P)
self fertilization/sexual
(not described)
(not described)
(not described)
(not described)
-/sexual
self-fertilization/sexual
(not described)
Gametic automixis (G)
~
White (1973)
Templeton (1982)
Bell (1982)
Asker (1980)
Crew (1965)
Lovis (1977)
Walker (1979)
Klekowski (1979)
Drebes (1977)
Fritsch (1965)
Bold & Wynne (1978)
Round (1973)
Fincham (1983)
Maynard Smith (1978)
Reference
Table 1. The nomenclature and reproductive status attributed in the literature to parthenogenetic (P) and gametic (G)
forms of automixis. The confusion evident in the table is described in the text
W
w
N
324
M.MOGIE
between the centromere and the first chiasma but heterozygosity will be
maintained for distal loci. If non-sister nuclei fuse (i.e. a x b) heterozygosity will
be preserved for loci situated between the centromere and the first chiasma but
may be lost for distal loci.
The distinction made above between allogamy, autogamy and automixis is
clear-cut. Regrettably, the definition of automixis has been extended to
encompass three further processes, none of which involve nuclear fusion (Mayr,
1963; Suomalainen, Saura & Lokki, 1976; Bell, 1982). Two of these involve a
reductional meiosis and endomitosis (during which the chromatids separate at
anaphase but cell division does not occur, the doubled set of chromosomes being
enclosed within the same nuclear membrane). In the first, meiosis produces a
haploid cell which undergoes endomitosis to give a diploid egg which is
homozygous at all loci and which develops parthenogenetically. In the second,
the diploid egg mother cell achieves tetraploidy by endomitosis; meiosis then
produces a diploid egg cell which develops parthenogenetically. During this
meiosis only sister (i,e. replica) chromosomes are thought to pair. If this is the
case then the progeny will be genetically identical to the mother, maintaining
any heterozygosity present; however, heterozygosity will be reduced if non-sister
(i.e. homologous) chromosomes occasionally pair. Maynard Smith ( 1978) does
not consider this last endomitotic process to be automictic, identifying it simply
as a form of thelytoky (a general term describing the parthenogenetic
production of female progeny by a mother). The third process is restitutional;
that is, following chromosome or chromatid separation during meiosis, the
separated derivatives are enclosed within the same nuclear membrane, giving an
unreduced egg which develops parthenogenetically. During this meiosis
chromosome pairing and crossing-over are thought to be normal; the genetic
consequences are therefore the same as those described for the fusion of two
tetrad nuclei. (Another reproductive process, ‘diplosporous apomixis’, also relies
on a restitutional meiosis but here restitution always occurs during the first
meiotic division and there is little or no chromosome pairing or crossing-over,
resulting in heterozygosity being maintained: see Nogler (1984) for a review of
apomictic processes.)
The taxonomic distribution of automixis
Several factors help to determine the capacity of an organism to reproduce
automictically, and the type of automixis to be expected. These include whether
the organism is isogamous or anisogamous and, if the the latter, whether or not
its life cycle contains a multicellular haploid stage. Isogamous organisms
produce only one morphological type of gamete, and each gamete may fuse with
any other unless incompatibility mechanisms intervene. Anisogamous organisms
produce different morphological type of gametes, which are often described as
male and female. Gamete fusion occurs between but not within morphs. In both
anisogamous and isogamous organisms the gametes are produced by the haploid
stage in the life cycle. In multicellular animals and in two algal groups (diatoms
and Fucus species) the haploid stage is unicellular and comprises the gametes;
mitosis is absent from this stage and the gametes arise through the
differentiation of meiotic tetrad cells. In anisogamous plants and fungi and in
isogamous organisms, the haploid stage is multicellular; here each tetrad cell
AUTOMIXIS
325
divides mitotically to produce a multicellular stage which generates gametes
(the cells comprising this stage may either associate to generate a multicellular
body, as in bryophytes, pteriodophytes, seed plants and many fungi and algae,
or each may exist as an independent unit, as in the confusingly named
‘unicellular’ fungi, algae and Protozoa). I n plants this haploid stage is called the
gametophyte, and this terminology will be adopted to describe this stage in all
organisms. Two types of gametophyte need to be distinguished for anisogamous
organisms. In the first, each gametophyte generates both gamete morphs; fern
biologists describe organisms producing this type of gametophyte as
homosporous and this terminology will be applied throughout (e.g. Klekowski,
1979). In the second, each gametophyte generates only one of the gamete
morphs; organisms producing this type of gametophyte will be described as
heterosporous. In heterosporous organisms each meiosis gives rise to only one
type of gametophyte and thus to only one type of gamete.
As stated, the type of life-cycle experienced by an organism has a considerable
influence on its capacity for automixis and on the type of automixis to be
expected. Isogamous organisms and homosporous anisogamous organisms may
undergo automixis by gamete fusion. Fusion may occur either between gametes
produced by the same gametophyte (intragametophytic automixis) or between
gametes produced by different gametophytes derived from different cells of a
single meiotic tetrad (intergametophytic automixis). I n each case automixis is
non-parthenogenetic, and will be facultative as gametes will also be able to fuse
with others derived from different meioses. Many organisms are either
isogamous or homosporous, including approximately 40 000 fungal species, 40%
of the 30000 bryophyte species, 90% of the 12000 pteridophyte species and
many of the 17 500 algal species. These forms of automixis may therefore be
common. However, intergametophytic automixis may often be precluded as the
haploid stage is often the main or only dispersal stage in the life-cycle of the
organism. The probability that two gametophytes derived from the same meiosis
will disperse into the same small area must be small, and most
intergametophytic fusions will be autogamic or allogamic. The dispersal strategy
of the haploid stage will not affect the incidence of intragametophytic automixis.
However this form will be precluded by the presence of self-incompatibility
systems. These are common within the fungi but intragametophytic automixis
has nevertheless been recorded in a number of species; unfortunately these are
typically described as examples of self-fertilization rather than of automixis
(Ingold, 1973; Fincham, Day & Radford, 1979). The incidence of selfincompatibility among the algae is unknown. However, it is thought to be
infrequent among the bryophytes and pteridophytes (Sporne, 1975; Smith,
1978; Klekowski, 1979), although this assumption is based on limited data and
self-incompatibility may be more common than assumed. Nevertheless,
numerous cases of intragametophytic automixis have been recorded in these
taxa although they are typically described as being autogamic rather than
automictic (Sporne, 1975; Page, 1979; Klekowski, 1979).
Gametic forms of automixis are precluded in heterosporous organisms (seed
plants, approximately 10% of fern species) and in those organisms with a
unicellular haploid stage (multicellular animals, diatoms and Fucus species). In
both groups each meiosis produces only one type of gamete and all fusions must
therefore be autogamic or allogamic. However, non-gametic, parthenogenetic
M. MOGIE
326
forms are not precluded, and have been recorded in diatoms, flowering plants
and insects. Automixis in diatoms is achieved by the fusion of first or second
division meiotic products to give a diploid egg which develops
parthenogenetically. It occurs facultatively with autogamy and allogamy and is
deemed to be a sexual process by Fritsch (1965), Round (1973) and Bold &
Wynne (1978), who, however, describe it as autogamic rather than automictic,
and by Drebes (1977) who describes it as being automictic (Table 1). However,
Drebes (1977) misuses the term, adopting it as a synonym for self-fertilization,
with the result that autogamic as well as automictic processes are defined as
automictic. Automixis in the flowering plants is achieved by the two endomitotic
processes described earlier (see Fig. 1) and by the fusion of cleavage division
nuclei of a parthenogenetically developing haploid egg. It occurs facultatively
with autogamy and allogamy and is considered to be an asexual process (see
Asker, 1980, for discussion and references). These processes are typically
described as being matromorphic rather than automictic (Table I ) , a situation
which has led Maynard Smith (1978) to state incorrectly that automixis is
absent from flowering plants, and Asker (1980), who believes ‘matromorphy’
2 n Embryo
I
Mitosis to
give
mu1ticel lulor
phase,
Endomito& during
EMC differentiation
.1
4 n EMC
I
Reductional
meiosis
Restitut ional
Reductionol
meiosis
meosis
Part henogenesis
Parthenogenesis
followed by
fusion between
cleavage division
nuclei
s
2n Embryo
Figure 1. Forms of parthenogenetic automixis in insects. The various types are fully explained in the
text. Briefly, meiosis may be restitutional or reductional. A reductional meiosis may be preceded by
an endomitosis, in which case reduction will restore the diploid number of chromosomes. If no premeiotic endomitosis occurs, then meiosis will give rise to haploid products. Here, diploidy may be
restored following restitution at the second meiotic division, by endomitosis or by fusion between
two of the tetrad nuclei. In all cases the diploid egg develops parthenogenetically. Alternatively, a
reductional meiosis may give rise to a haploid egg which develops parthenogenetically to initiate a
haploid embryo. Here the embryo achieves diploidy following the fusion of cleavage division nuclei.
EMC = Egg mother cell.
AUTOMIXIS
327
may be common, to state that it is rare. (Asker (1980) acknowledges the term
‘automixis’ but restricts its definition to encompass only the fusion of nuclei present
in the female gametophyte; forms involving the fusion of tetrad or cleavage
division nuclei, and forms involving restitution or endomitosis are described as
matromorphic.) Insects probably show the widest range of parthenogenetic
automictic processes of any taxonomic group. These are depicted in Fig. 1 and
include the fusion of tetrad or cleavage division nuclei, restitution and pre- and
post-meiotic endomitosis. The terminology used to identify these processes is also
variable (Table 1). They are described as automictic (White, 1973; Maynard
Smith, 1978; Bell, 1982; Templeton, 1982)’ apomictic (Templeton, 1982),
thelytokous (Crew, 1965; Maynard Smith, 1978) and parthenogamic (Crew,
1965). They are also variously described as sexual (Bell, 1982) and asexual
(Crew, 1965; White, 1973; Maynard Smith, 1978; Templeton, 1982).
Finally it should be stressed that organisms which are able to undergo
gametic forms of automixis may also undergo parthenogenetic forms. For
example, a number of homosporous ferns undergo the (pre-meiotic) endomitotic
form of automixis found in heterosporous flowering plants and in insects.
However, this is recognized as a form of apomixis (the Dopp-Manton scheme of
apomixis-Klekowski,
1973; and Table 1) rather than as a form of
parthenogenetic automixis (Lovis, 1977; Walker, 1979; Klekowski, 1973, 1979).
AUTOMIXIS AS A SEXUAL OR AN ASEXUAL PROCESS
In the previous section, attention was drawn to disagreements over the status
of automixis as a sexual or an asexual process. These disagreements involve
parthenogenetic forms; forms which involve gamete fusion are seen to be sexual
(e.g. Ingold, 1973; Smith, 1978). The extent of the disagreement over the status
of parthenogenetic forms can be seen clearly in Table 1 which also depicts some
of the terminological confusion relating to the description of automictic
processes. This latter problem need not be dealt with further. However, the
sexual or asexual status of automictic processes does require further
consideration, not least because parthenogenetic forms have been compared with
(sexual) allogamous systems in discussions of the relative advantages and
disadvantages of sexual and asexual reproduction (e.g. Maynard Smith, 1978;
Templeton, 1982). The conclusions resulting from these discussions may have to
be modified if these forms of automixis can be shown to be essentially sexual.
The disagreement surrounding the status of automixis largely results from the
lack of a generally agreed definition of what constitutes sexual reproduction.
Most of the numerous definitions given in the literature can be described as
functional or mechanistic. Functional definitions stress the genetic consequences
of reproduction rather than the processes involved, defining as sexual those
methods which result in the production of novel genotypes. For example,
Williams (1975) defines sexual reproduction as any process that involves nuclear
fusion or that fails to preserve the parental genotype including (as a ‘degenerate’
form) the “artificially induced development of haploid eggs”. Similarly, Daly &
Wilson (1983) define it as comprising any mode of reproduction that entails
fusion of gametes to produce a genetically novel offspring; asexual reproduction
is defined as comprising any mode of reproduction that does not entail fusion of
gametes and thus produces offspring genetically identical to the parent. These
328
M. MOGlE
two definitions of sexual reproduction are incompatible and both can be faulted.
Each implies that gametic fusion will automatically result in the production of
novel genotypes, which is simply not the case. It has been shown how certain
forms of automixis can produce fully homozygous progeny. If one of these
progeny then reproduced by (gametic) automixis or by autogamy then its
progeny would be genetically identical to itself and to each other. Daly &
Wilson ( 1983) also assume that parthenogenetic reproduction will always
replicate the parental genotype rather than generating novel genotypes. This is
obviously not the case for a heterozygous individual reproducing either by
haploid parthenogenesis or by any form of parthenogenetic automixis other
than that involving the pre-meiotic, endomitotic doubling of the chromosome
(discussed in previous section).
In contrast to functional definitions, mechanistic definitions emphasize the
processes involved in reproduction rather than their genetic consequences.
Sexual reproduction is defined as a process that involves meiosis and fertilization
(e.g. Darlington, 1958; John & Lewis, 1975; Fincham, 1983). For example,
Fincham ( 1983) defines sexual reproduction in eukaryotes as comprising
“. . . the fusion of nuclei . . . at one stage of the life cycle, resulting in a double
(or diploid) set of chromosomes, balanced at another stage by the restoration of
the single set (haploid) condition by the process of meiosis”. Here, the parentage
of the fusing nuclei and the nature of the resulting genotype are ignored. Such
definitions are more robust than are functional ones but they can still be faulted.
Thus Fincham’s (1983) definition excludes as a sexual process the fertilization of
meiotically unreduced eggs even though this event may occur sporadically in
most organisms, following an occassional breakdown of meiosis, and may have
been important during angiosperm phylogeny (Harlan & DeWet, 1975).
Occassionally, ontogenetic definitions appear. For example, Balinsky ( 1975)
claims that “. . . in sexual reproduction, the new individual develops from one
cell, the fertilized or parthenogenetically activated ovum”. This definition,
which eschews a requirement for meiosis and fertilization, and for the
production of novel genotypes, is probably unique in including diplosporous
apomixis as a form of sexual reproduction. It is certainly an easy definition to
apply, although it assumes all organisms are oogamous, and is generally
unhelpful.
These few examples are sufficient to illustrate the inconsistent way in which
reproductive processes are defined. How sexual reproduction should be defined
is a matter for debate, although a mechanistic definition would appear
preferable to a functional one, at least until the function (or functions) of sex has
been clearly delimited. Thus, no consideration should be given, in the definition,
to the genetic consequences of sexual reproduction. This is reasonable, both
because a single process, for example autogamy, can result in genetically novel
or genetically uniform progeny, depending on whether the parent is
heterozygous or homozygous, and because recombination may have evolved
primarily as a DNA repair mechanism rather than as a means of generating
novel genotypes (Maynard Smith, 1978). A suitable working definition can be
suggested. This is that all reproductive processes which involve nuclear fusion
are sexual, irrespective of the origin of the nuclei and of their (meiotically)
reduced or unreduced status, and irrespective of the nature of the resulting
genotype.
AUTOMIXIS
329
With this definition all forms of gametic automixis will be classed as sexual,
along with autogamous and allogamous processes, but so to would those forms
of parthenogenetic automixis which involve the fusion of tetrad nuclei. In each
of these processes a cell formed by the fusion of two nuclei goes on to develop
into a new individual. This form of parthenogenetic automixis differs from other
sexual processes only in that fusion (fertilization) occurs during egg development
rather than during zygote formation, requiring the automictic egg to
subsequently develop parthenogenetically. However, all other forms of
parthenogenetic automixis should be classed as asexual as the new individual
arises from a cell which has not been involved in a nuclear fusion event. This
includes that form of automixis that involves the fusion of cleavage division
nuclei. Here the fusion event is not associated with the generation of a new
individual but with the development of an existing individual generated
parthenogenetically from an egg cell.
REFERENCES
ASKER, S., 1980. Gametophytic apomixis: elements and genetic regulation. Hereditas, 93: 277-293.
BALINSKY, B. I., 1975. A n Introducfion to Embryology, 4th edition. Philadelphia: W. B. Saunders.
BELL, G., 1982. The Masterpiece of Nature. The Evolution and Genetics of Sexualio. London: Croom Helm.
BOLD, H. C. & WYNNE, M. J., 1978. Introduction to the Algae. New Jersey: Prentice-Hall.
CREW, F. A. E., 1965. Sex Determination. London: Methuen.
DALY, M. & WILSON, M., 1983. Sex, Evolution and behaviour, 2nd edition. Boston: PWS Publishers.
DARLINGTON, C. D., 1958. Evolution of Genetic Systems, 2nd edition. London: Oliver & Boyd.
DREBES, G., 1977. Sexuality. In D. Werner (Ed.), The Biology of Diatoms: 250-283. Oxford: Blackwell.
FALCONER, D. S., 1981. Introduction fo Quantifafive Gcnefics, 2nd edition. London: Longman.
FINCHAM, J. R. S., 1983. Genetics. Bristol: John Wright & Sons.
FINCHAM, J. R. S., DAY, P. R. & RADFORD, A., 1979. Fungal Genetics, 4th edition. Oxford: Blackwell.
FRITSCH, F. E., 1965. The Structure and Reproduction of the Algae, Vol. I . Cambridge: Cambridge University Press.
HARLAN, J. R. & DE WET, J. M. J., 1975. On 0.Winge and a prayer: The origins of polyploidy. The
Botanical Review, 41: 361-390.
INGOLD, C. T., 1973. The Biology of Fungi, 3rd edition. London: Hutchinson.
JOHN, B. & LEWIS, K. R., 1975. Chromosome Hierarchy. London: Oxford University Press.
KLEKOWSKI Jr, E. J., 1973. Sexual and sub-sexual systems in homosporous pteridophytes: a new
hypothesis. American Journal of Bofany, 60: 535-544.
KLEKOWSKI Jr, E. J., 1979. The genetics and reproductive biology of ferns. In A. F. Dyer (Ed.), The
Experimental Biology of Ferns: 133-1 70. London: Academic Press.
LOVIS, J. D., 1977. Evolutionary patterns and processes in ferns. Advances in Bofanical Research, 4: 229415.
.MAYNARD SMITH, J., 1978. The Evolution of Sex. Cambridge: Cambridge University Press.
MAYR, E., 1963. Animal Species and Evolution. Cambridge, Massachusetts: The Belknap Press of Harvard
University Press.
NOGLER, G. A,, 1984. Gametophytic apomixis. In B. M . John (Ed.), Embryology of Angiosperms: 475-518.
Berlin: Springer-Verlag.
PAGE, C. N., 1979. The diversity of ferns. An ecological perspective. In A. F. Dyer (Ed.), The Experimental
Biology of Ferns: 9-56. London: Academic Press.
ROUND, F. E., 1973. The Biology of fhe Algae, 2nd edition. London: Edward Arnold.
SMITH, A.J.E., 1978. Cytogenetics, biosystematics and evolution in the Bryophyta. Advances in Botanical
Research, 6: 195-276.
SPORNE, K. R., 1975. The Morphology of Pteridophytes, 4th edition. London: Hutchinson.
SUOMALAINEN, E., SAURA, A. & LOKKI, J., 1976. Evolution of parthenogenetic insects. Evolutionary
Biology, 9: 209-257.
TEMPLETON, A. R., 1982. The prophesies of parthenogenesis. In H. Dingle & J. P. Hegmann (Eds),
Evolution and Genetics of Lqe Histories: 75-101. New York: Springer-Verlag.
WALKER, T. G., 1979. The cytogenetics of ferns. In A. F. Dyer (Ed.), The Experimental Biology of Ferns:
87-132. London: Academic Press.
WHITE, M. J. D., 1973. Animal Cytology and Evolution, 3rd edition. Cambridge: Cambridge University Press.
WILLIAMS, G. C., 1975. Sex and Evolution. Princeton: Princeton University Press.