BULLETIN OF MARINE SCIENCE, 45(2): 433-446,
1989
TELLING SEX FROM GROWTH: DISSOLVING
MAYNARD SMITH'S PARADOX
John S. Pearse, Vicki B. Pearse and A. Todd Newberry
ABSTRACT
For nearly two decades, theoretical concern about the evolution of sex has centered on
Maynard Smith's paradox: Assume egg-production by parthenogenesis equals that by sex,
and assume that in a sexual species a female parthenogen appears by mutation. Initially, the
proportion of parthenogens will double in each generation - the "twofold cost of sex." And
yet, paradoxically, most species are overwhelmingly sexual. We suggest that there is no such
cost, and that the "paradox" results from an inappropriate comparison between two processes:
sex (anisogamous) and growth (clonal through ameiotic parthenogenesis). Unwarranted focus
on selection at the level of individual bodies (ramets), rather than on individual genomes
(genets) and genetic lineages, also has led to considerable confusion. Understanding the "uses"
of sex that account for its origin and persistence still stands as a major challenge to evolutionary
biology. But equating sexual reproduction with such disparate processes as clonal growth (by
ameiotic parthenogenesis, in Maynard Smith's paradox) is unlikely to illuminate the problem
of why sex itself is such an integral part of the biology of most organisms.
In 1971 John Maynard Smith published a paper in the Journal of Theoretical
Biology entitled "What use is sex?". His paper became the center of a controversy
in evolutionary biology that is only now being resolved. The title of Maynard
Smith's paper was startling enough by itself; sex was so familiar to everyone that
its "use" had been accepted by most biologists almost without question. As Trivers
(1985, p. 329) has pointed out, before Maynard Smith's paper " ... biologists
hardly knew there was a problem where sex was concerned. Since then a whole
new world has opened up." Indeed, most biologists of the time seemed comfortable
with the view, suggested by Weismann (1887) and developed by Fisher (1930)
and Muller (1932), that sex served to fix favorable mutations more rapidly in a
population than was possible without it-a decidedly group selection approach.
Maynard Smith (1971a) joined Williams (1966) in questioning the group selection
approach and showed that, to work, the available models of group selection needed
very large population sizes, even larger than those proposed by Crow and Kimura
(1965). On the other hand, he also showed that Williams's (1966) model gave an
immediate advantage to the individual only in highly fluctuating environments,
a condition that seemed too restrictive for the widespread occurrence of sex.
Maynard Smith (1971a, 1971b) proposed an alternative explanation that depended on the advantage gained when two populations invade a new environment
and mix through sex-also a rather unusual condition and not likely to account
for the near universality of sex.
By 1978 Maynard Smith had consolidated these views, arguing that the "use"
of sex remained an enigma, particularly when explanation was sought at the
individual level of selection. A large and well-developed literature has built up
over the past decade that addresses different aspects of what Williams (1975)
called the "paradox of sexuality" and Ghiselin (1987) termed "Maynard Smith's
paradox." And yet this abundant attention (reviewed by Lloyd, 1980; Bell, 1982;
Shields, 1982; Stearns, 1985; Ghiselin, 1987, 1988) has not provided a consensus
on Maynard Smith's question. We will not answer it, either. But we will propose
that Maynard Smith's paradox might itself be illusory and therefore unnecessary
to resolve.
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1989
THE PARADOX
Maynard Smith (1971a, 1971b, 1978) set up a "cost of sex" paradigm contrasting special cases of sexual and asexual reproduction. He used ameiotic (am ictic, apomictic) parthenogenesis as an example of asexual reproduction, because
it can be readily compared with sexual reproduction in the same species. The
model presumes that neither the number of eggs produced by an animal nor the
probability that the product of an egg survives to breed will depend on whether
that animal is a parthenogen or sexual. Because half the eggs of the sexual females
produce males, the proportion of parthenogens increases from n/(2N + n) to
n/(N + n) in one generation, where n = parthenogens and N = sexual animals
(both males and females). When n is small, the proportion of part he no gens in the
population will double in each generation, thus giving a "two-fold cost of sex."
In this view, the cost of sex is the cost of producing males (for sex) rather than
just females (for eggs). Of course, both males and females have babies; but sex
requires two individuals, one of each gender, in order to have those babies, while
a single female (the fecundity-determining gender) can produce them parthenogenically just by herself. Sex is thus only half as efficient numerically as parthenogenesis in producing offspring. And yet it persists.
Maynard Smith noted (1971 b; 1978) that isogamous sex incurs no such numerical cost. Indeed, in isogamous sex, as seen in unicells such as Chlamydomonas
(e.g., Bell, 1985), sexual reproduction (meiosis + syngamy) and asexual reproduction (mitosis) are numerically equivalent (Fig. 1). Thus, despite the widespread
belief that Maynard Smith's paradox of unequal progeny-production applies to
sex in general, he recognized that it can apply only to anisogamous species. It is,
in other words, a cost more of development than of sex; it is the cost of specializing
the egg. Because isogamy almost certainly preceded the developmental specializations of anisogamy, and the numerical cost of sex actually applies only to
anisogamous systems, Maynard Smith further acknowledged that his cost-of-sex
paradox does not apply to the origins of sexual reproduction. Recent discussions
about the origin of sex, none of which uses cost-of-sex arguments, can be found
in Halvorson and Monroy (1985) and will not concern us here. But does the costof-sex paradox apply even to the maintenance of sex? In fact, does the paradox
even exist?
OTHER
COSTS OF SEX
Other workers have proposed modifications of Maynard Smith's cost-of-sex
paradox. For example, Bell (1982), citing Williams (1975), advanced the view
that there is not only a numerical cost but also a genetic cost to sex. Because
outcrossed zygotes contain only half of each parent's genetic contribution, in
comparison to complete representation of the parental genome in asexual offspring, Bell (1982, p. 63) argues that "[t]he sexual female therefore propagates her
genome ... only half as efficiently as the asexual female." However, as Figure 1
shows, in isogamous species, alleles propagated sexually are as fully represented
among the subsequent zygotes as they are when propagated asexually. Thus, Bell's
case is again one about the developmental specializations (e.g., polar bodies) of
anisogamy. But, even in isogamy, does not sex dilute each parent's original diploid
genome to haploidy in anyone of its offspring, while mitosis keeps the parental
genome intact? Yes, but this difference between full allelic representation in the
parent versus half-representation in the offspring does not describe a genetic cost
of sex. Rather, it specifies the crux of sex: genome mixing.
Trivers (1985, p. 318) focused on differences in parental investment: "In the
PEARSE ET AL.: DISSOLVING MAYNARD SMITH'S PARADOX
(a)
ASEX
(b)
435
SEX
Figure 1. (a) Asexual reproduction, in contrast to (b) isogamous sexual reproduction in diploid
unicellular eukaryotes, The solid and open characters in the symbolic organisms represent alleles of
a designated genetic locus.
majority of species the female invests resources in each offspring, while the male
contributes nothing beyond his genes." Genetically, though, each sex contributes
equally to their offspring. Unequal, gender-biased contributions of resources to
zygotes or offspring once again mark anisogamous sex, or even gonochorism, but
are not intrinsic to sex per se.
There are, however, several apparently real costs of sex, isogamous or not.
There may be the cost of disintegrating successful genomes, a cost of meiosis
(Williams, 1975; Uyenoyama, 1984, 1985, 1987). This is not a baldly numerical
cost nor one involving proportions of subsequent allelic representation. Rather,
it is a more elusive measure of genomic adaptation. Sex appears to be a central
evolutionary gamble that splits the components of fitness, "survival and reproduction" (Futuyma, 1979), into an almost contradictory relationship. After all,
meiosis (recombination and segregation) destroys adaptively advantageous genotypes, breaking up favored gene combinations, including heterozygotes, and
syngamy produces new and untested genotypes, with consequent risks to the fitness
of the sexual offspring as compared to their parents' fitness. Mitotic reproduction
avoids the possible adaptive cost of genetic reorganization inherent in sex. Tendencies for inbreeding in many taxa may partially counter this "adaptive cost"
of meiosis and syngamy by maintaining gene combinations (Shields, 1982); these
tendencies seem to offer indirect support for the cost-of-meiosis hypothesis. But
Uyeno yam a (1984, 1985, 1987) concludes from mathematical analyses that inbreeding, whatever else its benefits and liabilities, does not necessarily reduce the
cost of meiosis and has little effect on the conditions that maintain biparental
reproduction.
We suggest that, in general, meiotic cost may not be very important. Consider
that in most cases of sex two well-adapted individuals are involved; at least, they
both have reached adulthood and succeeded in reproducing sexually. Moreover,
as Shields (1982) has documented, in many taxa sexually breeding individuals
are closely related. While some offspring receive less adaptive genotypes, others
may receive more adaptive genotypes. If, on average, the sexual offspring are as
well adapted as their parents, where is the cost?
One apparently unquestioned cost of sex is rarely (e.g., Lloyd, 1989) included
in "cost-of-sex" arguments. Energy and materials must be allocated to the production of gametes and the other attributes of sex rather than to other functions,
such as growth and maintenance. Sex can be a risky and expensive process that
adversely affects survival of an individual (Stearns, 1976, 1980; Kozlowski and
Wiegert, 1986; Sibly and Calow, 1986); in semelparous species, sex is lethal or
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BULLETIN OF MARINE SCIENCE, VOL. 45, NO.2,
1989
at least coincides with death. Without sex, an organism can increase its survivalfitness by directing energy and material resources to mitotic growth. And this
investment is one that repays: growth is the organism's chief means of securing
for itself still greater amounts of energy and resources. Sebens (1979) and Shick
et al. (1979), for example, have noted that growth translates into high fitness in
terms of eventual sexual reproductive success.
As these citations and our comments suggest, almost two decades have carried
the debate a long way from Maynard Smith's original formulation. But his paradox
is still a stimulus that sets many workers to search for other costs of sex and for
its uses, whatever its costs, that might account for its near universality at least
among metazoans and metaphytes. And so the alternative against which sex's
costs and uses are usually compared involves the costs and benefits of growthfor example, the numerical impact of parthenogenic cloning, the genetic conservatism of mitosis, growth's energetic costs and benefits. Not all organisms have
the same opportunities for investing in growth. Some, such as micrometazoans,
kamptozoans, or hydroids, have body-plans that are structurally or physiologically
size-limited.
Unicells
are especially size-limited.
Other species face ecological
limits-for example, space immediately available to bryozoans growing on a
patchy or ephemeral substrate or parasites growing in or on a host. Given such
varied circumstances, it is not surprising that organisms have evolved many modes
of growth, just as they have evolved many modes of sexual reproduction. We
shall consider modes of animal growth now, and then reconsider sex and Maynard
Smith's paradox with the added perspective a comparison ofthese developmental
patterns provides.
MODES OF GROWTH
The various modes of growth may be grouped broadly into several categories:
growth may be nonclonal (=aclonal) or clonal, and both of these may be unitary
or colonial (=iterative) (Table 1). Figure 2 depicts sexual organisms with various
ontogenetic patterns, nonclonal and clonal, the latter unitary or colonial, as summarized in Table 1. Each mode has advantages in different taxa and environments
both for the survival of a genome and, ultimately, for sexual reproduction. The
idea that colonies and clones are products of replicative growth of a single genome-that "asexual reproduction" is in fact a mode of growth-was seen by
earlier invertebrate biologists (Berrill, 1961; Mackie, 1963; Brien, 1966). However,
evolutionary biologists have only partially appreciated the consequences of this
view. Kays and Harper (1974) were among the first when they proposed for plants
that the connected modules of a colony or the dispersed units of a clone be termed
"ramets," ramifying units that together comprise a single "genet," which is genetically equivalent to a single, zygotically founded individual. The genet may
have unitary or colonial growth, or it may break up into a clone of unitary or
colonial ramets. This view has now gained wide acceptance for animals, as well
(Jackson, 1985; Jackson and Coates, 1986; Hughes, 1987a; Rosen, in press).
Propagation oframets may proceed by fission, fragmentation, or budding. Ameiotic parthenogenesis is also a way of proliferating ramets (e.g., Williams, 1986), in
which the egg serves as a unicellular bud. The distinction between ramets and
genets is bound to affect many ecological and evolutionary studies of clonal organisms and requires that we reexamine interpretations that have not accommodated this distinction. Thus, recognizing that populations of aphids and of
dandelions comprise many genetically identical ramets, but fewer different genets,
and that natural selection operates mainly at the level of genets, Janzen (1977)
cautioned that "the population ecology of aphids, like that of dandelions, is
virtually unknown."
PEARSE ET AL.: DISSOLVING
GROWTH
MAYNARD SMITH'S PARADOX
437
SEX
I
I
I
NONCLONAL
I
I
81H
I
M
I
I~
II
Z
gametes
I
CLONAL
I
I
I
I
I
I
I
I
I
Polyembryony
I
gametes
Z
Larval Replication
gametes
z
Adu~ Replication
z
z
gametes
BIH
Embryo(s)
BlH
M
Larva(e)
JuvfAdu~(s)
Embryos
Larvae
M
JuvfAdu~s
Figure 2. Schematic comparison of growth strategies in sexual organisms to onset of the first (in
semelparous taxa, the only) bout of sex in metazoans, with genets considered as whole life cycles and
independent ramets produced by replication during clonal growth. Each entire zygote-to-gametes
schema represents one genet; each horizontal line represents a ramet. In strategies with larval or adult
replication, retention of progeny produces colonial forms. Z, zygote; B/H, birth or hatch; M, metamorphosis.
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1989
Table I. Modes of growth in metazoans: a classification of the major ways of growing found among
animals, with examples.* Potential consequences for the genetic and population structure of members
of the 3 different major categories are enormous (see Figs. 2 and 3)
1.
Sexual and nonclonal
a) Unitary: genet = one unique, discrete body.
Some actinians, e.g., Anthopleura xanthogrammica; many turbellarians; most nematodes, molluscs, arthropods, echinoderms, vertebrates; solitary ascidians.
b) Modular and colonial: genet = one indivisible colony of physically and physiologically linked
modules.
Pennatulaceans, e.g., sea pansy Reni//a; some siphonophores, e.g., Physa/ia; a few
ascidians, e.g., Polyc/inum planum.
II.
Sexual and clonal
a) Modular and unitary: genet = many separate ramets, each a discrete body; ramets produced
by fission and budding.
Fission: some actinians, e.g., Anthopleura elegantissima; some fungiid corals, e.g.,
Diaseris; most scyphozoans (strobilation); many turbellarians, e.g., Microstomum.
Catenula, Dugesia; trematodes (polyembryony?); some polychaete annelids, e.g.,
Dodecaceria, syllids; a few echinoderms, e.g., asteroids Linckia, Luidia and the
ophiuroid Ophiactis.
Multicellular budding: most scyphozoans (stolons); a few hydrozoans, e.g., Hydra;
some fungiid corals, e.g., Fungia; loxosomatid kamptozoans.
Unicellular budding: orthonectid and dicyemid mesozoans (agamogony); some rotifers, many cladocerans, aphids and some other insects (ameiotic parthenogenesis).
b) Modular and colonial: genet = many separate ramets, each a colony of physically and physiologically linked modules; ramets produced mostly by fragmentation (either active or accidental) or budding.
Almost all bryozoans, hydroids, zoanthids, octocorals, pedicellinid kamptozoans;
most scleractinian corals; many pterobranchs, ascidians.
III.
Asexual and clonal
a) Modular and unitary: genet = many separate ramets, each a discrete body, in a lineage that
appears to be permanently without sex, growing endlessly by clonal replication.
Fission: a few triclad turbellarians; polychaete annelid Zeppe/ina; some asteroids.
Unicellular budding (ameiotic parthenogenesis): most rotifers; many terrestrial oligochaetes (earthworms); a few actinians, molluscs, tardigrades, cladocerans, ostracods, aphids, moths, fishes, lizards.
b) Modular and colonial: genet = many separate ramets, each a colony, in a lineage that appears
to be permanently without sex, growing endlessly by clonal replication.
Fragmentation: Panamanian lineages of the coral Poci//opora damicornis .
• In the terminology of Rosen (in press) la is "aclonal unitary," Ib is "aclonal iterative,"
"clonal
iterative";
however,
Rosen (in press) distinguishes
"iterative"
and "colonial"
lIa is "clonal unitary," and lib is mainly
growth plans while we have not, and we distinguish
"colonial" and "clonal" more sharply than hc. Hc does not include our catcgory Ill.
Research into the evolutionary pressures that produce the different modes of
nonclonal and clonal growth is now in considerable flux (Harper et al., 1986a;
Calow and Sibly, 1987; Hughes, 1987a, 1987b; Rosen, in press), at least partly
because of uncertainty about whether to focus on ramets or genets. But it is clear
at least that different environments favor different modes of growth, as much as
they favor different morphologies ofthe consequent bodies. It is readily accepted
that colonial growth allows for connected modules to replicate and spread both
in space and in time to secure large areas and attain extended longevities for the
genet (Harper, 1977, 1985; Kott, 1981; Hughes and Cancino, 1985; Potts et al.,
1985; Harper et al., 1986b; Mackie, 1986; Chornesky and Peters, 1987). Biologists
have been more reluctant to view clonal growth in this manner, because the ramets
of a clone are disconnected and often dispersed into "populations," prompting
comparisons with populations generated not by somatic growth but by sexual
reproduction; thus, clones can be treated as extended genets (Wallace, 1985) or
PEARSE ET AL.: DISSOLVING
MAYNARD SMITH'S PARADOX
439
demographically as individual ramets (Caswell, 1985) or modules (Begon et aI.,
1986), Deciding whether clonal replication of ramets should be treated as a form
of growth to be contrasted with other forms of growth, or as a form of populationgenerating reproduction to be contrasted with sexual reproduction, seems crucial
for understanding both the ecological consequences of growth and the "use" of
sex. We will now argue that clonal replication is better viewed as a form of
growth, and we will show the significance of this decision by applying it to Maynard
Smith's paradox.
Like organisms with nonclonal growth, those with clonal growth are adapted
to particular environments (reviewed by Bell, 1982). For example, Sebens (1979)
concluded from mathematical models that areas of poor food conditions favor
clonal growth in sea anemones (e.g., the facultatively cloning anemone Anthopleura elegantissima: see Smith and Potts, 1987). By clonal growth the anemones
maintain small ramet sizes, better able to glean what food is available, while at
the same time growing to large genet sizes. Under more favorable conditions with
large food items, genet growth without clonal replication produces a single large
nonclonal individual. In both cases, increase in size, whether as a large solitary
individual or as many small clonemates, has allowed the genet to maximize its
eventual production of gametes during sexual reproduction.
Many organisms with clonal growth are well known to characterize particular
habitats that favor small size. Tropical ophiuroids living in sponges and algal
turfs, for example, are typically small; there is no space for larger bodies. Many
of these species are fissiparous, so that a sponge or algal clump contains many
ramets of only a few genets (Hendler and Littman, 1986; Mladenov and Emson,
1988). Although the fecundity of anyone ramet may be low, the aggregate fecundity of all the clonemates could be very high. Similarly, freshwater hydras
have unitary clonal growth, producing many independent ramets that can rapidly
populate a confined habitat (Bell and Wolfe, 1985). When hydras become sexual,
individual ramet fecundity is low, simply because each polyp is so small, but the
entire genet's fecundity, again, is very high. Similar comparisons between low
ramet fecundity but high genet fecundity can be made with other sexual species
that have unitary clonal growth; parasites, such as trematodes, offer especially
striking examples.
Micrometazoans offer even more extreme cases of animals with the diminutive
bodies demanded by particular habitats. Most of these animals clone by parthenogenesis. Some, such as those usually used to contrast sexual and asexual
reproduction (Williams, 1975; Maynard Smith, 1978; Bell, 1982; Trivers, 1985),
are sexual species that regularly undergo sex only after some period of clonal
growth. These, like the ophiuroids and hydras mentioned above, may be viewed
as clonal species that can attain large genet sizes before undergoing sex, and
consequently, although their ramets are tiny, they can attain high genet fecundities.
In terms of both survival and sexual reproduction, such genets enjoy high fitness.
Others, such as most rotifers, some nematodes and tardigrades, and many protists,
are not known to have sex at all (Pearse et a1., 1987). These organisms survive
severe adversities including prolonged desiccation, and their dried bodies can be
carried on the wind; they may be viewed as huge asexual lineages dispersed on a
virtually global scale.
Figure 3 depicts the numerical consequences of the presence or absence of
clonality and sex. In this figure, each lineage of hypothetical organisms begins
with two genetically different individuals with a "fecundity" of 10 eggs per female
or parthenogen. In Figure 3-1 the sexual lineage is assumed to have a 1:I sex ratio,
and in Figure 3-11 50% of the eggs generated at the third parthenogenic event are
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1989
®
®
®
®
10-
50
250
1,250
Ramets
Genets
1,250
1,250
10,000
10,000
SEXUAL AND NONCLONAL
II
III
®
®
10
100
®
®
SEXUAL AND CLONAL
10
100
®
®
®
®
10
100
1,000
10,000
ASEXUAL AND CLONAL
10
100
20,000
1,000
2
10,000
Figure 3. Comparison of increase in number of independent ramets (bodies) and number of genets
(genetically distinct organisms) after four "generations" of propagation with the differing growthstrategies that provide the three basic groupings in Table I: [I] sexual & nonclonal, [II] sexual & clonal
(where cloning is by parthenogenesis), and [Ill] asexual & clonal (where cloning is by parthenogenesis).
The circled p's and S's denote parthenogenic and sexual events, respectively. The numbers indicate
the progeny resulting from each propagative event, parthenogenic or sexual, assuming a parthenogen
or female fecundity of 10 eggs and a I: I sex-ratio in sexual events. We begin and thus end 3-Ill with
two "genets," not two ramets of a single genet, to expedite comparison with 3-1 and 3-Il; in fact,
defining "genet" in asexual lineages is an unresolved difficulty, but not one that negates the lesson to
be drawn from comparing the genetic and population consequences of these three growth-strategies,
as discussed in the text.
PEARSE ET AL.: DISSOLVING
MAYNARD SMITH'S PARADOX
441
assumed to grow into males preparatory to sexual reproduction, The circled P's
and S's denote occurrences of parthenogenesis and of sex, respectively, The numbers indicate the progeny resulting from each of the four propagative events, be
it parthenogenic or sexual, in each schema. Note that while four parthenogenic
bouts (Fig. 3-III) produce the highest number of ramets, they produce no new
genets. When sex finally occurs after three cycles of parthenogenic clonal growth
(Fig. 3-II), each parthenogen of the original pair has grown to 1,000 ramets, with
a combined fecundity of 10,000 (half the sexual participants being males), while
a nonclonal female genet has a fecundity of only 10 at the time of any sexual
bout. Although hypothetical, these models may be compared, for example, to
different groups of rotifers: in the class Digononta, all members of the order
Seisonidea are sexual and nonparthenogenic and all members of the order Bdelloidea are asexual and parthenogenic; in the class Monogononta (including most
species of rotifers), all are parthenogenic with only about 10% known to have sex.
Our view that nonclonal and clonal organisms result from variations of the
same phenomenon-growth-follows
from the well-established idea in both developmental and evolutionary biology that an organism is a whole life cycle
comprising the mitotic progeny of a zygote. That is, an organism is an entire
ontogeny (de Beer, 1958; Bonner, 1965, 1974; Williams, 1966, 1975; Gould, 1977;
Harper, 1977; Arthur, 1982). Thus, in species that are ever sexual, an entire genetic
organism, or genet, persists from its beginning in syngamy through all its developmental manifestations, including asexual replication of ramets, until its death.
In this view, new genetic individuals-new
life cycles-appear in sexual species
only through sex, and their production can therefore be considered a "use" of
sex. An individual, in this sense, is not just any kind of independent body, but
only a genet. In sexual species with clonal modes of growth, the production of
new genetic individuals (genets) is not equivalent to the production of clonemates
(ramets). Consequently, analyses of the "cost of sex" that rely on a bare comparison
ofthe numbers of progeny-the essence of Maynard Smith's paradox-risk comparing disparate entities: ones that are ramets of genets versus ones that are entire
genets. These progenies are not equivalent populations.
SEX, ASEXUAL LINEAGES, AND LEVELS OF SELECTION
Among the different kinds of life cycles, only those that include clonal growth
provide a means for genetic individuals (genets) to escape sex and death by being
or becoming permanently asexual lineages. In such lineages that lack sex altogether, genets and even species are difficult to delineate, a seldom approached but
widely recognized problem (Mayr, 1963, 1969; Ghiselin, 1975; Hull, 1976). Asexual lineages are not uncommon, but their scattered taxonomic distribution (at
least among multicellular taxa), generally with closely related sexual taxa, suggests
that any particular one has a limited evolutionary future (reviewed by Maynard
Smith, 1978; Bell, 1982). On the other hand, bdelloid rotifers form an exceptionally large and diverse order entirely comprised of asexual lineages; in this,
they "constitute a real problem for evolutionary biology" (Maynard Smith, 1978,
p. 69; see also Mayr, 1963).
Comparing sexual species with such asexual lineages inevitably invites group
selection paradigms, as developed by Crow and Kimura (1965), Felsenstein (1974),
Stanley (1975), and a reluctant Maynard Smith (1978). These may be unnecessary
if the "individual" on which selection acts is defined as the genet and ifan asexual
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1989
clone is considered as one such genet, albeit dispersed among many physiologically
independent entities (Janzen, 1977; Williams, 1988).
However, entities even above the genet level still may form important units of
selection. For example, Lynch's (1985) analysis of mutation rates in obligately
parthenogenic cladocerans indicates that mutation by itself would allow significant
rates of phenotypic evolution in asexual lineages, but that sex tremendously enhances the rate of phenotypic evolution - up to about five times the rate achieved
by mutation alone. Case and Taper's (1986) comparison of sexual and asexual
competitors, using mathematical models, also essentially at a group selection level,
shows that sex increases species niche width, reducing intraspecific competition
and offsetting the "reproductive advantage" of the asexual species. These findings
lead Case and Taper to conclude (p. 385): "The much-vaunted capacity of asexual
species to produce twice as many reproductive individuals per generation may
turn out to be somewhat ofa red herring .... " Similarly, after arguing that poorly
developed genetical theory early in this century hampered understanding and
development of evolutionary theory, Ghiselin (1987) concluded (p. 658), "It is
still unclear how much genetical theory, perhaps including Maynard Smith's paradox, will prove equally artifactual." On the other hand, current models to explain
the adaptiveness of sex (e.g., "penny stock," "Red Queen," "tangled bank," reviewed by Bell, 1982; Stearns, 1985; and Ghiselin, 1987, 1988) may still apply
when sexual and asexual lineages are compared, for the problem ofthe persistence
or "use" of sex remains. But Maynard Smith's paradox, which fails to distinguish
ramets from genets, while once provocative, may now be merely distracting.
SEX VERSUS GROWTH
We noted earlier (as in fact did he) that Maynard Smith's paradox does not
apply generally to sex, but only to anisogamy. Moreover, the paradoxical advantage of the alternative to sex is even more limited: it applies only to anisogamous
organisms with ameiotic parthenogenesis, a relatively rare mode of clonal increase,
and does not apply even to the anisogamous organisms that have other, far more
common modes of asexual replication. The many kinds of fission, fragmentation,
and budding summarized in Table 1 and Figure 2 apparently are practiced equally
by males and females, of which almost all continue to engage in sex also, without
engendering any paradox. Furthermore, among those few ameiotic parthenogens,
which the paradox predicts should abandon sex and become exclusively parthenogenic, many have indeed done so (Table 1), and mixed populations of a sexual
species and its asexual derivatives may well be in the process of doing so. Where
then is the paradox?
Ironically, the key to the problem of sex may lie in the observation that most
permanently asexual lineages of animals in fact do maintain themselves by parthenogenesis and not by other asexual modes of growth. We suggest that what
permits obligate parthenogens to persist is not the purportedly great efficiency
with which they pass on their genome intact. Fission, for example, would do as
well or better (and does, among asexual protists such as amoebas). On the contrary,
it may be that the one-celled bud-the parthenogenic egg-provides an asexual
multicellular organism with the only stage in which a favorable mutation can
occur and be integrated through development (Buss, 1987). This could well provide the lineage with the diversity essential to natural selection and evolution. As
has been long recognized (Muller, 1932), evolution is bound to be slower in an
asexual than a sexual lineage, and this lag would contribute to the rarity of asexual
PEARSE ET AL.: DISSOLVING MAYNARD SMITH'S PARADOX
443
lineages in animals and account for their surviving only in particular sorts of
habitats. In fact, identifying the essential characteristics of habitats that promote
or sustain asexual lineages may help us finally to understand the significance of
sex.
CONCLUSIONS
1. Numerical, genetic, and parental investment "costs of sex" are actually specialized costs of anisogamy, and have little to do with the origin or maintenance
of sex in its fundamental sense. The main problem with these proposed "costs"
is their failure to recognize ameiotic parthenogenesis as a form of donal growth,
which functions in sexual species to greatly enhance the genet's fecundity.
2. The meiotic cost of sex may be a real "cost of sex" in the sense of decreasing
a genet's reproductive fitness by breaking up favorable genetic combinations.
Because it is sometimes countered by tendencies toward selfing and inbreeding,
there is evidence that sex inherently decreases "fitness." But if offspring have on
average the same fitness as their parents, the meiotic cost of sex also may not be
generally important.
3. The resource allocation cost of sex, while not induded in most "cost of sex"
arguments, apparently is the only unquestioned cost; it detracts from growth and
maintenance, and therefore from survival. In this view, growth is a process separate from sex, and both compete for resources. Growth takes several forms
(nondonal and donal, unitary and colonial), and the adaptive value of these
different forms can be contrasted in ecological and evolutionary terms. Because
sex produces genetically new individuals in most eukaryotes (and all multicellular
forms), it provides for a continuity of gene flow in forms with nondonal growth.
It may be a prerequisite for the evolution of multicellularity. Clonal growth has
the potential to continue indefinitely without sex; understanding the conditions
that allow obligately asexual donal species to persist may help lead to an understanding of the "use" of sex.
4. Although Maynard Smith's paradox has generated valuable insights into
epiphenomena or consequences of sex, there is no paradox if sex is not equated
with donal growth (by bald demography of nonequivalent items). Nor may the
argument that sex is a result of selection on individual bodies have much relevance
to the origin and maintenance of sex, if, as in organisms with donal growth, those
bodies are ramets, not entire genets. Sex generates new genets in a gene pool,
somehow enabling the gene pool to continue through time. Without sex (that is,
in asexual lineages) genets and gene pools are synonymous. We believe that the
"use" of sex will be better understood within a context of strict distinction between
modes of growth and of sex, consequently between ramet and genet, and also
between genet and gene pool. A more thorough study of the biology of asexual
lineages may advance this search for understanding.
ACKNOWLEDGMENTS
We thank J. Bonner, C. Chaffee, K. Fischer, N. Foltz, L. Francis, M. Ghiselin, L. Goff, J. Maynard
Smith, C. Otis, M. Haley, D. Lindberg, S. Raay, P. Steinberg, R. Trivers, J. Wourms, four anonymous
reviewers, and particularly R. Buchsbaum and D. Potts for stimulating criticisms of this and earlier
manuscripts and for other valuable assistance. Some of these colleagues will continue to disagree with
parts of the present essay. We also thank B. Rosen for providing us with his manuscript still in press.
We are particularly grateful to the late Professor D. P. Abbott, who admonished so many students,
444
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1989
including us, that the animals themselves are the authorities, and that when there is disagreement
between what our theories say and what the animals do, one should pay more attention to the latter.
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DATEACCEPTED: October 25, 1988.
ADDRESS: Institute of Marine Science and Biology Board of Studies, University of California. Santa
Cruz. California 95064.