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AMF.R. Zooi... 19:739-751 (1979).
Apomictic Parthenogenesis and the Pattern of the Environment
KARI VEPSALAINEN AND OLLI JARVINEN
Department of Genetics, University of Helsinki, P. Rautatiekatu 13,
00100 Helsinki 10, Finland
SYNOPSIS. Advantages of obligatory apomixis are modeled, and curculionid weevils are used
as examples. It is suggested that the alleged twofold number of female offspring in relation
to sexual parentals should not be exaggerated. Instead, specific circumstances facilitating
the origin of especially heterotic genotypes capable of apomixis should be sought; crosses
between differentiated (long-isolated) populations (preferably followed by a population
flush) seem promising. Optimal strategies in temporally heterogeneous environments are
studied, and situations favoringsexual reproduction both in fine-grained and coarse-gained
environments seem common (apomicts are capable only for individual adaptability, but
sexual populations may track even one-generation changes by evolving). In apomicts,
diapause determination and other seasonal constraints need specific attention, as they may
interfere with geographical dispersal, and only life-cycles of one or more years seem
possible. In rich biotic communities, which evolve continuously, evolutionary rigidity of
apomicts may lead to their extinction. This shows that the dichotomy between immediate
and long-term advantages of apomixis needs revision; if the number of generations needed
for competitive exclusion between asexual and sexual organisms is relatively high, the
greater evolutionary potential of sexual populations must be considered (there are directional changes both in the physical and biotic environments). Apomixis then seems most
advantageous in low-competitive, early succession habitats which are recurrent and change
relatively slowly (increased colonization ability of apomicts is here advantageous). Also,
apomixis may succeed in spatially coarse-grained environment in stable patches small
enough to exclude high-competitive community at the site. Then reduced vagility (loss of
flight) may facilitate the origin of apomixis.
INTRODUCTION
The well-known biological paradox is,
"What use is sex?" In the history of life, the
transition from asexual to sexual (or meiotic) reproduction has certainly taken a long
time. On the other hand, the evolution of
cloning, which dispenses with meiosis and
results in the production of genetically uniform offspring, has occurred quite recently
in many lineages (see Williams 1975: 111).
As modern modes of cloning are derived
from sexual modes of reproduction, we
here prefer to compare the advantages of
the evolutionarily more advanced condition with those of the more primitive one;
we thus rather pose the question, "What use
is apomixis?" Indeed, why has a system like
apomixis evolved many times in higher
plants and animals? It is true that apomixis
may double the number of female off-
VVe thank Prof. Esko Suomalainen and Seppo
Kuusela for helpful discussion.
spring, but they are nevertheless copies of
each other.
In apomictic parthenogenesis only one
maturation division takes place in the egg,
and this is an ordinary mitosis. As no bivalents are formed and there is no reduction
division, the zygoid chromosome number
and the whole genome is maintained unchanged in apomicts (Suomalainen, 1962).
Our paper is focused on obligatory
apomixis; for example, cyclic parthenogenesis presents quite different problems.
As will be seen, it is necessary to take into account the historical origin of parthenogenesis and the environmental pattern
in studying apomixis as an adaptive strategy. Our main examples refer to curculionid weevils (Coleoptera), which have
been thoroughly studied by Suomalainen et
al. (1976, and references there). In weevils
many species have evolved apomixis
(Suomalainen, 1969), though these apomictic derivatives represent a minority among
Curculionidae, which is the largest family
of insects with over 60,000 species. Gener-
739
740
KARI VEPSALAINEN AND OLLI JARVINEN
ally, the parthenogenetic invertebrates
occur as isolated cases among the sexual
species (Enghoff, 1976).
ORIGIN OF APOMIXIS
Williams (1975) made the point that the
existence of long-term advantages should
not be used to explain the biological significance of sexual reproduction. He also
suggested that it is largely the difficulty of
adopting the asexual mode of reproduction
that prevents man and many other slowly
reproducing species from becoming asexual. As many weevils have evolved apomixis, the main evolutionary problem in
this group is evidently not finding a proper
cytological mechanism for reproducing
asexually. Instead, there must be specific
ecological and/or historical mechanisms
which have favored apomixis in certain
cases, but which have maintained sexual
reproduction in others.
Many asexual weevils1 have a wide distribution while the "sexual races" and many
closely-related sexual species are restricted
to smaller areas (Suomalainen, 1969). As a
typical example, Otiorhynchus scaber L. is
widely distributed in northern Europe, but
the sexual "race" only occurs in scattered
localities in the Alps. As emphasized by
Suomalainen (1969; cf., also Seiler, 1961),
these localities correspond to areas known
to have been ice-free during the Wiirm
(Wisconsin) glaciation. We agree with the
conclusion by Suomalainen (1969) that the
origin of apomixis in weevils dates back to
the times after the glaciation, when the ice
cover began to retreat. We conjecture that
the small, long-isolated beetle populations
could gradually expand, and crossings between individuals of highly differentiated
populations must have followed.
1
Because the apomictic individuals do not form a
Mendelian population, the terms "population," "race,"
and "species" are vague in this context. An apomict
"population" is formed by phenotypically similar individuals (biotypes), which occupy a restricted area, and
a "race" or "species" consists of a system of closely
related biotypes which occupy a geographical range
equivalent to that of a species (Timofeeff-Ressovsky et
at., 1969).
These crossings have most probably led
to increased heterozygosity in the offspring
populations. This postulate is supported by
Suomalainen and Saura (1973) who suggested that the very high heterozygosity in
sexual O. scaber (0.31, or higher than in
practically any other sexual organism
studied; cf., Powell, 1975) is due to crossings
between differentiated populations,
though it is not clear whether historically
remote phenomena are valid explanations
for the presently high heterozygosity.
We do appreciate the potential twofold
reproductive capacity of apomicts as compared with sexual genotypes, but this point
should not be exaggerated. Indeed, there
are indications that asexual strains do not
fully utilize this potential (examples in
Enghoff, 1976: 37). Instead of stressing the
allegedly high reproductive capacity of
apomicts, we argue that their success lies in
maintaining exceptionally successful genotypes. These are rarely formed in sexual
populations, but they are faithfully copied
in cloning.
We suggest that a major mechanism in
producing unusually favorable genotypes is
by hybridization between long-isolated
populations. The hybridizing populations
may also belong to different species, though
this does not seem to be a general rule
(Suomalainen e£a/., 1976). In normal sexual
populations no individuals are much more
heterozygous than the average (Sved et ai,
1967), but very high heterozygosity does
result from hybridization. Apomictic "mutants" arising in hybrid populations are
thus expected to be very heterozygous
compared with individuals in the parental
populations. Of course, the mutants surviving probably represent the very best mutants, as survival probability of mutants increases with mutant fitness (e.g., Fisher,
1930; Templeton, 1977). The competitive
ability of apomictic mutants may be further
enhanced by the increased recombinational
load, including "hybrid breakdown," in the
sexually reproducing populations.
It is not certain whether hybridization of
long-isolated populations is a necessary
condition in the origin of apomixis, but the
mechanism suggested here seems quite
plausible. We think that a major difficulty in
APOMIXIS AND PATTERN OF ENVIRONMENT
establishing the apomictic mode of reproduction is that the apomictic apparatus
(cytological mechanisms, reproductive physiology, courtship behavior, etc.) is not immediately faultless. In consequence, failures in utilizing the reproductive potential
must initially be compensated by high
fitness due to causes other than the advantage of not producing males. The historical
setting envisioned for the origin of apomixis is furthermore especially favorable for increases of heterozygosity. As
understood by Chetverikov (1905, 1926)
and Elton (1924) and finely formulated by
Carson (1968), there is an interplay between the ecological environment, population demography, and genetic variability;
post-glacial sexual populations of weevils
must have experienced a population flush
during which selection pressures were
relaxed and heterozygosity flourished.
Population flush may also have been
conducive to the survival of apomictic
mutants. It is also conceivable that—especially in slowly dispersing animals such as
the curculionids —the vast geographical
areas, which became gradually uncovered
after the retreating ice, offered greater
colonization success for apomicts (for the
advantages in colonization, as well as for
environments favoring apomicts, see
below).
HETEROSIS OF APOMICTS
Our emphasis of the highly heterozygous origin of apomixis is based on the idea
that high heterozygosity confers heterosis
(e.g., Lerner, 1954; Kirpichnikov, 1974); we
thus suggest that the function of parthenogenesis in weevils is largely to preserve
heterotic genotypes (cf., also Templeton
and Rothman, 1978). Interestingly, Hebert's (1978) studies on daphnids render
additional support to the importance of
heterotic genotypes. In intermittent populations, characteristic of temporary ponds,
Daphnia species reproduce apomictically
for two or three generations, after which
they produce eggs sexually. In such habitats, genotypic frequencies at polymorphic
enzyme loci were normally in good agreement with Hardy-Weinberg expectations.
741
In permanent populations, on the other
hand, where most clones reproduce by continued apomixis, genotypic frequencies
showed an excess of heterozygous individuals and, in some cases, populations consisted entirely of individuals heterozygous
at one or more loci.
Our hypothesis thus suggests that high
heterozygosity occurs in apomictic lineages
from the origin. One diploid apomict has
been studied electrophoretically in curculionids, Polydrusus mollis Strm. Observed
heterozygosity was 0.36, which differs
sharply from the value for the sexual population, 0.14 (Saura et al., 1977). Another
explanation of the high heterozygosity in
apomictic lineages is that heterozygosity increases owing to mutation pressure (e.g.,
Suomalainen, 1969). This effect was modeled, though for a restricted class of mutations only, by Lokki (1976a). As it may be
assumed that the European apomictic
weevils have originated at the time of the
recent glaciation, there seems to be no
doubt that the mutation pressure has had
time to increase heterozygosity in these
apomicts, but the exact effect is unknown
for several reasons. For example, too few
data exist on mutation rates, and the model
of Lokki (1976a) does not consider realistic
selective effects. There is no contrast between our suggestion of high heterozygosity
from the origin and the suggestion by
Suomalainen (1969) and others that heterozygosity will increase owing to mutation
pressure. The point is, to what extent can
the existence of apomictic lineages be understood without the hypothesis of originally high heterozygosity?
Polyploid apomicts were also modeled by
Lokki (1976b). He observed that mutation
pressure tends to increase heterozygosity in
polyploids, but this prediction is hard to
test, as polyploids are expected to be highly
heterozygous in any case. If a triploid curculionid arises by chance fertilization of a
diploid apomictic female (e.g., Suomalainen,
1969), heterozygosity should be quite high
compared with diploids (see Lokki, 19766).
The data available (e.g., Saura et al., 1977)
fall well within the range expected on the
basis of the mechanism producing polyploids. None of the about ten cases studied
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KARI VEPSALAINEN AND OLLI JARVINEN
requires more complicated explanations
than this.
Lokki (1976b) suggested that triploids
and tetraploids have the special advantage
over diploids that heterozygosity "increases
very markedly within the same period of
time" compared with diploidy. As this process is nevertheless measured in units of /LIT1
(where M is mutation rate), the main selective advantage of triploidy and tetraploidy
rather seems to be their initially high degree of heterozygosity (and thus heterosis).
This explanation is supported by the fact
that of the 54 apomictic "races" and
"species" of weevils studied, not more than
two are diploid, while 31 are triploid and 14
tetraploid (Suomalainen et al., 1976). Several other mechanisms can, however, act in
the same direction.
Lokki (19766) pointed out that polyploids
are well buffered against deleterious mutations (to be accurate, he only considered
non-functioning alleles assumed to affect
survival and reproduction only in homozygous condition). As the probability of obtaining a recessive homozygote through
mutations is extremely low and as only a
single individual is eliminated in such a
process, the buffering effect can be important only if it is assumed that many mutations are non-recessive • (not necessarily
dominant). Considerable selection against
diploidy may then exist, the average number of deleterious mutations per genome
per generation being probably almost one
as in Drosophila melanogaster Meigen (Mukai
et al., 1972; Dobzhansky et al., 1977:71).
This account needs, however, modification as equilibrium is approached, but it
is a slow process. No true equilibrium arises
in the model by Lokki (1976a, b), as his
model focuses on a single lineage continuously represented by one individual. This
single representative must, sooner or later,
perish because of accumulated mutations,
but in more realistic models an equilibrium
is possible. This equilibrium results in a
mathematically calculated mutation load
due to deleterious mutations. At equilibrium, polyploidy involves a greater mutational load than diploidy, unless all mutations are completely recessive. For a similar
comparison between haploidy and dip-
loidy, see Crow and Kimura (1970: 316).
Of course, this is a long-term consideration, while the advantage of transition to
polyploidy is felt immediately.
A further point is that polyploid organisms tend to be more robust than diploids (Suomalainen, 1969). For example,
cold-hardiness of polyploid Otiorhynchus
dubins Strm. exceeded that of diploids in the
experiments by Lindroth (1954). Robustness may explain why polyploid animals
and plants are more common in areas recently uncovered by retreating ice sheets
(e.g., Suomalainen, 1950; Stebbins, 1971).
Robustness of females compared with
males in many animals may also contribute
to the adaptiveness of parthenogenesis
(White, 1973; Enghoff, 1976). In any case,
if robustness of females is an important factor in explaining the occurrence of apomixis, it almost automatically follows that
polyploids are expected to be frequent
compared with diploids.
We conclude that polyploidy is likely to
increase heterosis especially by improved
physiological homeostasis (Schmalhausen,
1946), and is thus generally advantageous
for apomictic forms, but the main unsolved
problems lie in the origin and maintenance
of parthenogenesis. We have above established a plausible mechanism for the generation of apomixis, and we now turn to consider its maintenance.
CHARACTERISTICS OF APOMICTIC WEEVILS
The main differences between apomictic weevils and their parental sexuals seem
to be the following, provided that differences exist (for secondary costs of sexual
reproduction, see Daly, 1978):
(1) The apomicts have the advantage of
not producing males, but the exact increase
of female offspring is not known (theoretically it may be doubled, and r may increase).
(2) As males are not needed, apomicts
can colonize more easily than sexually reproducing individuals (e.g., Suomalainen,
1969; White, 1973). This advantage is enhanced by the "oogenesis-flight syndrome,"
which is very common in sexually reproducing insects (see Johnson, 1966), dispersal
thus commonly occurring before mating.
APOMIXIS AND PATTERN OF ENVIRONMENT
Interestingly, a number of parthenogenetic
forms, e.g., the Otiorhynchus weevils, have
originated in species which have lost part of
their colonization ability (e.g., wings may be
reduced or totally absent, see Enghoff,
1976). See also point (1) above.
(3) Apomictic individuals are able to tolerate wider fluctuations of the physical environment (wider homeostasis is alleged by
high levels of heterozygosity).
(4) As no reorganization of the genetic
material occurs in apomicts, the offspring
of each female consist of genetically identical individuals. (To be accurate, the genotypes of the individuals of the same clone
differ slightly owing to mutations.) The
great stability of the genotype in apomicts
prevents rapid evolutionary responses to
environmental changes, as the ability to respond depends on the amount of additive
genetic variance in fitness (Fisher, 1930).
We wish to contrast the almost lacking
evolutionary response of apomicts with
their very rapid demographic responses. In
sexual populations demographic responses
are slower owing to Mendelian reshuffling
of genes among genomes at the population
level (cf., Thompson, 1976).
Apomicts thus have definite advantages
and it may be useful to specify an optimal
environment for them. A competitive community is clearly not the best community for apomicts (see also Glesener and
Tilman, 1978), as high specialization is favored there (Schmalhausen, 1946), which
means that energy allocation to homeostatic
devices against the physical environment is
minimized (of course within the limits of
the general organizational level of the
group). It has been shown also by Williams
and Mitton (1973) that competition decreases the advantages of apomixis.
The disadvantage of apomixis in competitive communities (including predators
and parasites) is perhaps best understood in
the context of the Red Queen's Hypothesis
by Van Valen (1973). As competitive communities contain many species, success is
possible only if a population is able to evolve
with the other populations forming the biotic environment. As the capability of response to selection requires considerable
genetic variance in fitness, sexuals are pre-
743
ferred to apomictic "populations," though
population is used here in a figurative sense
only. This conclusion follows because only
little genetic variance occurs in apomicts.
The low genetic variance of apomictic
populations is a fact documented by electrophoretic data (see Suomalainen et al.,
1976), but it is also easy to understand
theoretically. The only way apomicts can
respond to selection is that favorable mutant clones are selected. Coexistence of very
many different mutants is prevented by the
principle of competitive exclusion, as
pointed out by White (1973). So if a lucky
mutant arises, it is likely to outcompete
others; the establishment of favorable mutants thus results in genetic impoverishment, as a single superior clone replaces
inferior ones. Although many neutral mutants may theoretically coexist (Crow and
Kimura, 1970), the possibility is thus not
important because favorable mutants also
occur from time to time.
The above reasoning leads to the expectation that wide areas are dominated by occasional lucky mutants, an expectation
which is borne out by facts (Suomalainen et
al., 1976, and references there). A correlation between phytogeographic zones and
genotypes in Otiorhynchus scaber was demonstrated by Saura <>£«/. (1976), and these authors regard their results as a proof that
parthenogenetic lineages are capable of
evolution. We do not question this conclusion, but prefer another emphasis. As the
three genotypes, each dominating one of
the three phytogeographic zones studied,
differed only at one out of 22 loci studied,
apomicts showed minor divergence compared with the response shown by plant
communities. These results then show that
parthenogenetic populations almost totally
lack means of selective response.
As environmental heterogeneity counteracts specialization, the role of competition is likely to diminish in less stable environments (see Schmalhausen, 1946; MacArthur, 1972). Less stable environments
are thus favorable for apomicts, provided
that their individual homeostasis is sufficient for the new environments. Early
successional environments are favorable
for the apomictic mode of reproduction.
744
KARI VEPSALAINEN AND OLLI JARVINEN
First, these support a low-competition points. Els are highly subdivided, their
community, either because the area has parts being usually called individuals; but
been primarily uncovered after, e.g., the Els have very long lives and very low popuretreating ice of the last glaciation, or sec- lation growth rates. The resources harondarily, the high-competition community vested by dandelions or weevils are tempohas been destroyed by some environmental rary and unpredictable in exact location,
catastrophe, e.g., fire or human activities. but predictable in quality. Two of Janzen's
This selects for high r and colonizing poten- observations on dandelions help undertial. Second, successional environments are stand weevil problems.
predictable in the sense that similar habitats
(1) The multiplication of layman's inditend to recur at different places, and many viduals should not be confused with popuof these change but slowly. Hence, succes- lation explosions, for sudden increases in
sional environments can be invaded by a population size have genetic and evolutioconstant strategy, but the species must be nary implications, while within-clone mulable to colonize new environments.
tiplication has no such importance.
(2) Janzen predicts that each El probThe characteristics of apomicts thus seem
especially suited for early successional envi- ably occupies a natural habitat to the excluronments, provided these are not too sion of other evolutionary individuals. Each
short-lived. On the other hand, rapid suc- El should be locally adapted owing to incession, as e.g., the dung environment of terclonal competition, "a competition in
many beetles, poses a severe competition which the most locally adapted [El] graducommunity, and the microhabitat variation ally ends up as the nearly unremovable resbetween dung patches is great (Koskela and ident." As pointed out above, this is literally true of weevils. The areas dominated by
Hanski, 1977).
It has been pointed out by Saura et al. single clones naturally depend on dispersal
(1977) that the chrysomelid beetle Bromius ability. For example, in contrast to many
(adoxus) obscurus L. is an inhabitant of early apomictic Otiorhynchus weevils which lack
successional environments; the Eurasian flight ability, Bromius obscurus disperses
apomictic form feeds onfireweed(Chamae- widely by flight. Suomalainen et al. (1976)
nerion angustifolium (L.) Scop.) which dis- sampled Bromius individuals from 52 popuperses rapidly to habitats formed after for- lations over an area extending 1500 km in
est fire or clear-cutting. In contrast, Saura length. About 20 enzyme loci were studied:
et al. (1977) stress that, e.g., the weevil one genotype comprised 80% of all indiPolydrusus mollis is a climax species. This viduals and was the only genotype in most
contradiction to our emphasis is, however, populations. Bromius thus shows larger geonly apparent, for these weevils inhabit netic homogeneity at wider areas than the
particularly hazel (Corylus L.) bushes and flightless O. scaber (above).
young oak (Quercus L.) trees. Likewise, O.
scaber weevils live on young Norway spruce,
RESPONSES OF APOMICTIC ORCAN ISMS IN A
usually not higher than three meters, and
TEMPORALLY HETEROGENEOUS ENVIRONMENT
they rarely intrude more than some tens of
meters into the forest from the edge of the
We have concluded that apomictic
forest or a clearing (E. Suomalainen, per- weevils show a slow evolutionary response
sonal communication). Of course, young to environmental changes; favorable mutatrees are typical successional habitats, and tions can be occasionally established, but, in
they surely provide temporary, but spatially general, there is little genetic variance for
recurrent environments, which possess selection to act upon. Starting from the clashighly predictable characteristics.
sical model of population structure, Crow
We suggest that the strategy of apomictic and Kimura (1965; for a semi-stochastic
weevils is similar to that of Janzen's (1977) version, see Kimura and Ohta, 1971)
dandelions. Janzen introduced the concept showed that mutants are more rapidly esof evolutionary individual (El), which is a tablished in small asexual populations than
clone, in order to emphasize his basic in similar sexual populations. In their
APOMIXIS AND PATTERN OF ENVIRONMENT
model, sex accelerated evolution only if effective population size was large, rate of
favorable mutations high, and the individual selective advantage of mutants small.
As this argument is not relevant if most of
adaptive evolution is based on shifting frequencies of alleles already present in the
population (see Crow and Kimura, 1969),
we do not consider their results further.
The grain and range of the environmental
pattern
As all environments change, we now consider the basic responses of apomictic organisms to temporal heterogeneity in the
environment. In addition to the evolutionary response, which takes place at the
population level, responses at the individual level are possible; Ricklefs (1973) distinguishes between regulatory, acclimatory,
and developmental responses. In order to
understand these responses in relation to
apomixis, we need to consider different
patterns of environmental change.
The environment may change finegrainedly; the local optimum strategy is
then monomorphism of one phenotype,
though Mendelian constraints may prevent
in sexual populations the acquisition of
such an optimum (Levins, 1968). The degree of homeostasis is important: Effective
homeostasis may filter potentially harmful
environmental signals (in the terminology
of Schmalhausen, 1946, it would be more
or less autonomous regulative develop 1
ment). Templeton and Rothman (1978)
pointed out that previous models on the
evolutionary advantages of sex are based
on coarse-grained environmental heterogeneity. They showed that apomicts will
out-compete sexually reproducing individuals in fine-grained environments,
when there is sufficient heterosis, and/or a
sufficient loss of the secondary disadvantages of sexual reproduction, to overcome
the between-generation fitness variability.
This model thus predicts that apomicts
living in fine-grained environments are
heterotic; this prediction is supported,
though in a general way only, by the high
heterozygosity of apomicts at enzyme loci
(Saura et al., 1977). It has been concluded
745
that the segregation load in Mendelian
populations is an essential part of the adaptive strategy, by which populations adapt
closely to the environmental conditions
prevailing at any time (Schmalhausen,
1946; Istock, 1978). This conclusion is supported by the theoretical result of Templeton and Rothman (1978), as they showed
(see above) that the apomicts must, heterotically or by other means, be able to overcome the relative disadvantages caused by
the temporal fluctuations of local optima,
or otherwise sex is more advantageous.
Notice that this argument does not refer to
long-term changes in the environment.
The environment may also show autocorrelation. If so, the present environment does provide signals predicting the
future environment of the developing individual, which, if the autocorrelation is
sufficiently strong (Levins, 1968), favors
dependent development (Schmalhausen,
1946), and phenotypes varying as continuous functions of environmental signals are
produced (Levins, 1968). The probability
of apomixis is decreased in such environments, as apomicts have a very ineffective
genetic memory. Strictly speaking, they are
not capable of storing information about
environmental sequences.
Related (parental) sexual populations
may also gain advantage in competitive interactions during unfavorable periods for
apomicts. It has been shown by Roughgarden (1972) that asexually reproducing
populations respond more rapidly to environmental changes than sexuals, and this
conclusion contrasts with our inference.
The opposition is, however, only apparent,
as Roughgarden's model implies similar
additive genetic variance in fitness in the
populations compared. As stressed above,
this premise is invalid in apomicts, though it
may apply to other types of asexual reproduction (e.g., cyclic parthenogenesis). The
same notion applies also to Maynard
Smith's (1978: 102) model, where 32 asexual genotypes coexist, adapted to each of
the possible patch types. Such models do
not fit apomictic weevil "species" and
"races," which were each considered by
Suomalainen et al. (1976), on basis of enzyme genetic data, to have originated from
746
KARI VEPSALAINEN AND OLLI JARVINEN
one parental apomictic female.
As the range of offspring phenotypes is
likely to be wider in sexual populations than
in asexuals (e.g., Williams, 1975: 14), and
this difference should be especially striking
between sexuals and apomicts, sexual reproduction is expected to be the rule in
coarse-grained environments which show
great between-generation variation. However, if the between-generation variation is
unpredictable, tracking changes in the
physical environments may in fact be even
disadvantageous (Levins, 1964; Levin,
1975).
Coarse-grainedness always implies uncertainty. One way to reduce spatial uncertainty is by increased vagility; habitat selection is another way. High vagility is typical
for Lepidoptera (with about 165,000 recorded species), where, with the exception
of psychids, parthenogenesis is extremely
rare (Suomalainen, 1978). Still another way
to reduce spatial grain is to sit tight at a
favorable patch. When the patch is relatively stable, reduced migration rates may
be favored, and flightlessness selected for in
extreme cases. If the patch is sufficiently
small to avert high-competition communities at the site, apomicts are likely to
outcompete their sexual parental forms, as
in apomicts the favorable genotype is not
lost in meiotic segregation. Indeed, most
parthenogenetic derivatives of Lepidoptera have occurred in species with flightless
females. For example, the psychid moth
Solenobia triquetrella Hb. is wingless and in-
habits low-competition habitats. Suomalainen et al. (1976) suggest, on the basis of
enzyme genetic data, that parthenogenesis
has originated several times in this species.
Solenobia performs meiosis, but according
to Saura et al. (1977) there is no recombination, and the automixis is then functionally equivalent to apomixis.
Seasonal and geographical patterns
In connection with environmental predictability, seasonal fluctuations in the environment deserve emphasis, especially because they seem to have been neglected in
discussions on the adaptive significance of
sexual reproduction. Seasonal fluctuation
has selected for effective responses in animals, e.g., diapause systems. Many insects
are facultative diapausers, which react to
absolute and/or changing daylengths and
temperatures (by autoregulative development of Schmalhausen, 1946), but threshold values vary geographically. Geographic
variation tends to be striking, and the
diapause mechanisms of different populations have been shown to be adaptations to
local conditions. For examples on the behavior of "diapause races," see, e.g., data
on the moth Acronvcta rumicis L. (Danilevskii, 1961).
The switch mechanism for diapause
seems to depend on a small number of loci
with two or more alleles (for a review, see
Hoy, 1978). The silk moth (Bombyx mori L.)
is the best studied species in this respect,
and its diapause behavior seems to be regulated by three sex-linked alleles and three
autosomal genes (Lees, 1955). Moreover,
genes not only affect diapause determination, but also the duration of the diapause,
the "day-degrees" required for diapause
termination, and the cold-hardiness during
the diapause (Hoy, 1978).
Considering diapause mechanisms is of
utmost importance in evaluating the possibilities of different populations to extend
their ranges. In each apomictically reproducing lineage, diapause systems are liable
to interfere with dispersal to new geographical areas, especially as regards the
South-North axis, but, as longitudinal differences in climate exist, this effect is by no
means restricted to latitudinal expansion.
Colonizing new areas may be easy for demographic reasons for apomicts (above), as
they are not hampered by the oogenesisflight syndrome and they do not need males
for fertilization, but the life cycle may impose heavy constraints. Adaptation to seasonal environments is in apomicts then a
real problem, and they probably succeed
best in univoltine populations requiring at
least one but preferably several years to
complete their life cycles. This requirement
is fulfilled in the apomictic weevils studied
this far (e.g., Spessivtseff, 1923; Thiem,
1932; Takenouchi, 1959; Klingler, 1959;
APOMIXIS AND PATTERN OK ENVIRONMENT
and E. Suomalainen, personal communication), as well as in parthenogenetic SO/WO/MY;
moths (E. Suomalainen, personal communication).
The fine-tuning to the seasonal cycle implied by multivoltinism seems a very important condition selecting strongly against the
apomictic mode of reproduction. If the unpredictability caused by the rich biotic
community is a cause for the low frequency
of apomicts in the tropics compared with
regions recently uncovered by ice sheets
(Glesener and Tilman, 1978), then the local
fine-tuning of the life cycle to the seasonal
environment at higher latitudes is one important reason why apomixis is nowhere a
common strategy for animals. The seasonal
argument is clearly not valid for cyclical
parthenogenesis. On the contrary, parthenogenesis and sexual forms as well as seasonal cyclomorphoses are regulated by day
length in many multivoltine aphids
(Danilevskii, 1961).
We conclude that the theoretical advantage of apomicts in producing more females may be irrelevant in many natural
environments. In poorly autocorrelated
environments, the inability of apomicts to
cope with great between-generation fitness
variability may be fatal (this is especially
true when the environmental range exceeds individual tolerance), and the subtleties of seasonal environments (including
local yearly differences; for an example, see
Istock, 1978) may annihilate the theoretical
advantage of apomixis. It is a fact that the
demarcation line between univoltinism and
multivoltinism need not be a striking environmental discontinuity (for example, we
have studied voltinism in water-striders
Gerris Fabr., and many subtle patterns
emerge; see Vepsalainen, 1974, 1978; Jarvinen and Vepsalainen, 1976). Finally, there
is an obvious point: apomicts do have a low
upper limit for the rate of adapting to new
environments by evolving. This rate largely
depends on population size, average advantage of favorable mutants, and the frequency of favorable mutants (Crow and
Kimura, 1965), as local genetic variation is
not extensive (e.g., Saura et ai, 1977; this is
also theoretically expected, as pointed out
747
above). When the environment (physical
and/or biotic) changes at a higher rate than
apomicts can evolve, sexual populations
may still survive.
APOMIXIS AND GROUP SELECTION
The different survival probabilities of
apomictic and sexual populations lead us to
the problem of group selection. In his recent book, Maynard Smith (1978) states
that, in its simplest form, the group-selectionistic argument for the prevalence of
sexual reproduction runs as follows:
"An individual female which abandons
sexual reproduction obtains thereby an
immediate short-term advantage. This advantage means that once a parthenogenetic
strain is established, it will selectively displace the sexual species. In the long run,
however, the new parthenogenetic species
is doomed to extinction because of its inability to evolve. While parthenogenetic species
go extinct, sexual ones speciate, thus maintaining the total number of species. The
result of this process is that, at any time,
most species are sexual."
We believe that this is a good summary.
Certainly, we wish to question the assumption of immediate twofold advantage of
asexuality, as historical factors may be decisive in the origin of parthenogenetic
strains. As pointed out above, the success of
apomictic lineages may in fact be due to
other advantages than the theoretical twofold advantage in reproductive capacity.
We thus suggest that very few apomictic
lineages are able to establish themselves,
and in the long run they face extinction due
to their almost total lack of evolutionary
adaptability. (This lack of adaptability is not
absolute, as stressed by Suomalainen et al.,
1976). Looking at the process of evolution,
however, we suggest that individual selection acts the chief role. It is simply a process
of eliminating unfit genotypes, and if the
environment changes sufficiently, then an
inordinate proportion of the unfit genotypes will be those determining apomixis.
It is true that this process can also be
described as group selection, if group selec-
748
KARI VEPSALAINEN AND OLLI JARVINEN
don is defined as differential survival of
groups having different gene frequencies,
but in the present case group selection does
not provide any conceptual difficulties.
(The present case is equivalent to interspecific competitive exclusion.) Longterm group selection can also be modeled
and compared with short-term phenomena. Van Valen (1975) really estimated the
equilibrium frequency of apomictic angiosperms as 0.008. His model gives the relation s = 120/x, where 5 is the relative disadvantage of apomicts in extinction, and
H is the rate of production of apomicts from
sexual species. However, an important
point is that it is not implied by us that the
function (see Williams, 1966:9) of sex is to
prevent future extinctions. On the other
hand, we do imply that fitness values
change with time, but this assumption is
certainly sound. For example, it is one of
the fundamental lessons of the fossil record that most genotypes flourishing at one
moment in the geological history have by
now become extinct.
We need, however, more data on the relationship between group extinction and
the reproductive system. Apomicts may
well have low extinction rates, as a single
female may continue the clone. Extinction
probability of apomicts -is also decreased
by their (allegedly) high reproductive capacity.
In evaluating group selection, we also
wish to point out that the dynamics of the
system depends on the time scale. It is true
that long-term advantages of sex are problematic from the evolutionary point of view
(Williams, 1975), but we should have better
estimates of the number of generations
needed before a successful apomict lineage
can really outcompete a sexual strain. If
competitive exclusion requires a great
number of generations, the competing
populations will change evolutionarily, and
this may tip the balance in favor of the sexual population. The ability to estimate correctly the period required for competitive
exclusion makes it possible to compare this
time interval with the rate of evolution of
the biotic community and the probability of
important directional changes in the physical environment.
CONCLUDING REMARKS
Our discussion of apomictic weevils may
be summarized briefly by stating that in this
view apomicts are opportunist lineages,
which have succeeded in fixing a genotype
whose fitness has been very high at some
point of time. In successful cases, the cost of
apomictic opportunism is that they are
evolutionary dead-ends compared with
sexually reproducing species, though they
certainly have some possibilities to adapt
(Suomalainen et al., 1976). That this ability
to evolve is nevertheless very limited is
shown by "the absence of speciation and
further divergence in parthenogenetic
forms" (Suomalainen^ al., 1976).
There are several specific points which
we suggest should be studied in greater detail in the future.
(1) The fate of newly-arisen mutants is
determined during the first few generations, and the fate depends, e.g., on the
fitness value conferred by the new mutant
(Fisher, 1930; Templeton, 1977). In consequence, the origin of the apomictic mode
of reproduction should be given a thorough consideration. There are no grounds
for supposing that the transition to apomixis is a simple process (for reviews of
the cytological complications, see, e.g.,
Suomalainen, 1969; Suomalainen et al.,
1976; White, 1973). We would also like to
repeat the point made by Schmalhausen
(1946, and stressed also in the name of one
of his earlier books): Any specific adaptive
change of a feature must coadapt to other
features and their functions to be of value to
the organism as a whole. Thus the number of
ova producing females is only one aspect of
fitness, and other fitness features, e.g., viability from egg to adult, speed of development, efficiency in energy harvesting and
allocation of energy, length of breeding
season, timing of breeding (e.g., diapause
determination), habitats and micropatches
where offspring are laid, etc., are also important. The sexual mode of reproduction
may combine all these features (which may
vary in different times and different sites) in
some individuals, but apomicts must include them all instantaneously when transition to asexual reproduction takes place.
APOMIXIS AND PATTERN OF ENVIRONMENT
(2) If it is true that the advantage of not
producing males is annihilated by the less
than perfect functioning of the newly acquired apomictic system, other factors need
to be invoked in explaining why apomictic
lineages are sometimes established. We
suggest that considerable heterosis may be
the most important factor in explaining the
successful origin of apomict mutants. Simply, we imply that the decreased short-term
evolutionary adaptability is (partially) compensated by high individual adaptability in
successful apomicts. If so, new experimental data on heterotic effects in apomicts are
badly needed.
(3) Apomictic organisms should be studied ecologically. Of special interest are
their habitats, for there are indications that
a typical habitat in which apomicts succeed
is a relatively slowly and gradually changing, low-competition environment, which
is nevertheless recurrent. Early successional habitats often have these features.
Another point of interest is the life cycle.
Facultatively multivoltine populations
must be able to interpret correctly local environmental cues in order to diapause
properly (neither too late nor too early),
but the possibilities for local adaptation are
meager in apomicts. Longer life cycles (one
year or more) seem thus a condition which
is relatively more favorable for apomixis
(but which does not always liberate the organism from seasonal constraints).
(4) The problem of extinction of different lineages needs more studies. In this respect, better data are necessary as regards
fitness variation between generations. The
dichotomy of immediate vs. long-term advantages may also need revision, as the
evaluation of the dynamics of competition
between asexual and sexual organisms depends on the number of generations during which the two reproductive systems
coexist. If the number of generations is relatively high, the greater evolutionary potential of the sexual system must be considered (directional changes in the physical
environment, changes in the biotic community).
749
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