REVIEWS
Ancientasexualscandals
Olivia P. Judson and Benjamin B. Normark
I
n the past 25 years, theories to
Asexual organisms that are descended
to be unable to account for them.
explain the prevalence of sexual
from ancient asexual lineages defy
Further, until recently, empirical
reproduction have proliferated;
current thinking on the evolution of sexual
methods for evaluating claims of
according to one classification,
reproduction; theoreticians have been
ancient asexuality have been unanxious to explain away their existence.
satisfactory. This review, therefore,
20 hypotheses have been put forward’. However, the question can
However, a number of groups of organisms,
falls into three parts. First, we will
be turned around: if sex is necessfrom ferns to rotifers, have been suggested
examine several theories of sex to
ary - for whatever reason - how do
to be anciently asexual, and favourable
see whether they can allow for
some organisms manage to be evidence is being accumulated. FuHhermore, ancient asexuals. Second, we will
asexual? This question has been
new techniques for assessing claims of
round up the ancient asexual susasked by Gerritsenz, who examined
ancient asexuality have been proposed.
pects and present methods for dethe geographic distribution of parAlthough ancient asexuals challenge
tecting whether a putative ancient
thenogenesis to see whether the concurrent theories of sex, understanding
asexual is, in fact, ancient. Finally,
ditions where asexuals are found
how they manage to persist will help to
we willbriefly consider the evidence
are simply those where the cost of
explain why most organisms are sexual.
for three cases. For definitions of
finding a mate is too great for sexrelevant terms, see Box 1.
uals to be able to persist. Stearns”
Olivia Judson is at the Dept of Zoology, University of
also recommended that theories
Theoretical difficulties
Oxford, South Parks Road, Oxford, UK OX1 3PS;
to explain sexuality should be able
Some theoreticians have reBenjamin Normark is at the Dept of Ecology and
to account for parthenogens. But
sponded to the challenge of ancient
Evolutionary Biology, Biological Sciences West,
the question goes beyond underasexuals by doubting their existUniversity of Arizona, Tucson, AZ 85721, USA.
standing geographic parthenogenence6. For example, Hurst etal6pre
esis. After all, if an asexual lineage
posed that asexual lineages in which
appears,
it
might
flourish
initially;
no
males have ever been seen may
.
.
. .
but it it simply disappears again in a few generations, asexsimply be having sex too infrequently for them to be readily
uality has failed as a long-term adaptation. However, some
observed, and that asexual lineages may be frequently spun
asexual organisms appear to be descended from ancient
off from an undetected sexual species. Alternatively, asexuals
asexual lineages. The bdelloid rotifers are the most notorimay have other mechanisms of genetic exchange7. However,
ous, prompting Maynard Smith to write ‘the bdelloids
if ancient asexuals truly have no genetic exchange of any
remain something of an evolutionary scandal’d, but they are
kind, they raise the question of whether current theories of
not the only example (see below). In our view, the persissex can account for them. Broadly speaking, three hypotheses
tence of anciently asexual organisms poses a powerful chalto explain sex - the ‘Red Queen’, ‘Miller’s ratchet’ and the
lenge to all theories of sex.
‘mutation-load-reduction theory’ - have attracted particular
However, little theoretical work has focused explicitly on
attention in recent years. We will examine each in turn.
the persistence of ancient asexuals; current theory is thought
Asexuals and the Red Queen
The Red Queen states that sex is an adaptation to escape
from parasite+. Under the Red Queen, obligate asexuality is
Box 1. Relevant terminology
believed not to be viable because coevolving parasites are
Asexual: Reproducing(or an organism that reproduces) without sex,
thought to be able to adapt their strategies for infiltrating
such that the genetic material of each individual is derived from only one
parent. Asexual organisms may have no meiosis at all in their life cycles,
host defencesg. As asexuals often stay genetically the same
and reproduce by mitotically derived single cells (apomixis) or mitotically
through successive generations unless mutations occur (see
derived somatic tissues (vegetative reproduction). Alternatively, there
below), over several generations an obligately asexual linmay be a modified meiosis and ploidy restoration (automixis).
eage should accumulate coadapted harmful parasitesg. As a
Ancient asexual: An asexual organism descended from a lineage that
has reproduced by exclusively asexual means for a long stretch of
result, sexuals should be able to outcompete asexuals, be
evolutionary time.
cause the benefit of escape from parasitism should more than
Parthenogenesis:
Development of a new individual, either male or
compensate for the lower reproductive potential. However,
female, from an unfertilized egg. In this review, parthenogenesis should
dispersal in space or time has been suggested to function as
be taken to mean thelytoky - that is, the development of females by
an alternative to sexlo, and could be a way for organisms to
either apomixis or automixis.
Apomixis: Reproduction by single cells that are mitotically derived.
escape from parasite@. Ladle ef ~1.7examined whether disMeiosis does not occur, and each offspring is genetically identical to
persal in space could allow asexuals to escape from their
its parent (unless mutations occur).
parasites. They found that a large asymmetry between host
Automixis: Reproduction by single cells that are derived from a single
and
parasite dispersal enabled asexuals to outcompete sexparent by meiosis and restoration of ploidy. There are various automictic
mechanisms; their genetic consequences range from genetic identity
uals despite attack from parasites. Further studies showed
of offspring with parent to enforcement of complete homozygosity in
that in the regions where asexuals were able to outcompete
each generations.
sexuals, they were also able to maintain high levels of genAllele: In a diploid sexual or automictic individual, an allele is one of
etic
variationll, a result that agrees with data from natural
two homologous DNA sequences that pair and then segregate during
populations of asexuals.
meiosis. In an apomictic individual, an allele is one of two (or more)
homologous DNA sequences that functioned as alleles in the ancestral
sexual population. Thus, within apomictic lineages ‘allele’ is a historical
concept, like ‘homology’.
rREE uol.
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no. 2 February
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Asexuals and MDller’s ratchet
Miiller’s ratchet is thought to be a problem in small
populations rather than large ones because only in small
0
1996, Elsevier Science Ltd
41
REVIEWS
and Gabriel14have gone on to show that if fitness is determined by complex, polygenic traits, then a compensatory mutation - that is, a mutation that restores the original phenotype not by recreating the original nucleotide sequence, but
by some other means such as a mutation in a different gene
that influences the same trait - in a quantitative character
could mask the effects of the ratchet; however, it is not clear
that their results would hold over a very long time.
Other ways to evade the ratchet have also been suggested. Asexuals are often polyploid, and Mogie and Ford’s
showed that increased levels of ploidy could slow down the
ratchet. KondrashovlG demonstrated that if epistatic selection pressures are sufficiently strong, Miiller’s ratchet
might stop altogether and asexual lineages could persist indefinitely. Gabriel et ~1.17have argued further that if Miiller’s
ratchet is a problem for asexuals, it is not clear why the
DNA
of organelles such as miTable 1. Putative ancient asexual cladesa
tochondria or chloroplasts Estimated age No.
which are arguably ancient
Reproduction
Refs
(evidence)b
speciesC
Glade
asexual lineages - does not
seem to suffer from its effects.
populations is the least mutated class likely to be eliminated
by random genetic drift; in a small asexual population, the least
mutated class, once lost, cannot be brought back if backwards mutation is rareI*. However, the relative importance
of Mfiller’sratchet is unknown, and a number of mechanisms
(besides large population size) that might arrest the ratchet
have been suggested. Two are obvious (and also apply to
the mutation-load-reduction hypothesis, below): if the mutation rate per locus is low, or if the number of genes in the
genome is small, the mutation rate per genome will be reduced and Miiller’s ratchet will be slowed or stopped. Other
ratchet-slowing mechanisms are more subtle. For example,
Gabriel and Wagner13 found that in spite of high mutation
rates the advance of the ratchet depends on the balance between the strength of selection and random drift. Wagner
Taxonomic affiliation
Plants
Pteridophyta: Vittariaceae
Pteridophyta: Hymenophyllaceae
Vittaria sp.
Jrichomanes sp.
Fungi
Zygomycota: Zygomycotina
Glomales
Agaricales: Lepiotaceae
Agaricales: Tricholomataceae
‘Gl’ ant symbiontsd
‘G2’ ant symbiontsd
Animals
Rotifera
Nematoda:
Arthropoda:
Arthropoda:
Arthropoda:
Heteroderidae
Ostracoda
Anostraca
Atari
Bdelloidea
Meloidogyrte spp.
Darwinulidea
Artemia parthenogenetica
frotogamase//us
Geholaspis
Jrachytes
Lordalycidae
Haplochthoniidae
+ Pediculochelidae
Nematalycidae
+ Proteonematalycidae
Oehserchestidae
+ Granjeanicidae
Alicorhagia
+ Stigmalychus
Pomerantziidae
Lohmanniidae
Trhypochthoniidae
Malaconothridae
Camisiidae
Nanhermannidae
Nothrus
10 (geographic)
10 (geographic)
1
1
400 (molecular,
fossil)
>25 (fossil)
?
130
>35
?
70 (fossil)
30 (molecular)
?
?
?
?
363
4
26
1
6
6
5
8
?
?
vegetative (gemmae)
vegetative (gemmae)
27
27
azygospores
55
vegetative (ant culture)
vegetative (ant culture)
28
28
apomictic
apomictic
apomictic?
automictic/apomictic
?
?
?
?
29,30
31
32
33
34
34
34
34
?
4
?
34
?
15
?
34
?
13
?
34
?
?
?
?
?
?
?
?
7
7
5
24
20
32
12
24
?
?
?
?
?
?
?
?
apomictic
apomictic
apomictic
gynogenetic
hermaphrodite
hybridogenetic
34
34
34
34
34
34
34
34
35
35
36
37
Arthropoda: Homoptera
Tramad
?
11
Arthropoda: Coleoptera
Mollusca: Bivalvia
Neotramad
Aramigus tessellatus
N.E. Pacific Lasaea
?
2 (molecular)
4 (molecular)
6
~1
l?
Chordata: Teleostei
Poeciliopsis MO/II clade
0.1 (molecular)
~1
38
aOnly multicellular organisms are considered (although the list is not exhaustive); obligately asexual higher taxa may be
more common in bacteria and protists. For instance, no evidence of sexuality has been found for 27 out of 59 phyla of
protoctistazs. However, the mechanisms and extent of gene exchange in unicellular organisms can be difficult to determine6.25.26. This table includes (1) putatively exclusively asexual higher taxa (genera or higher) having more than two species,
and (2) any other lineages for which an explicit claim for ancient asexuality has been made and no contradictory evidence
has been found.
bEstimated age is given in millions of years. Listed ages are conservative: if a range of estimates exists, the lowest is given.
The nature of the evidence for the date is briefly indicated: geographic, fossil or molecular.
~1 indicates that sexual populations have been assigned to the same species, but a claim of ancient asexuality has
nonetheless been made for a particular lineage.
dThese putative ancient clones have obligate associations with ants. These associations have been likened to agriculture,
with ants tending their asexual crops (fungi) or livestock (honeydew-producing aphids). Myrmecophily may permit the
persistence of asexual lineages either by reducing the selection acting on them (e.g. if the ants remove parasites) or by
increasing the selection on them (e.g. if the ants prey differentially on less viable individuals).
42
TREE
Asexuals and the
mutation-load-reduction
theory
However, even if Miller’s
ratchet can be arrested, asexuals should still be subject to
the accumulation of slightly
deleterious mutations. Unlike
the ratchet, this should apply
in populations irrespective of
their size. Crow’s has called
this theory the ‘mutationload-reduction theory’. By this
theory, sexual populations are
able to remove a larger number of mutations over time
and thereby are able to reduce
their mutation load more rap
idlylJs. One strong prediction
can be made from this theory:
if the genomic mutation rate
is as much as one mutation
per generation, then some
mechanism to reduce the
mutational load is necessary.
Gabriel et cd.17have suggested that asexuals could
avoid the accumulation of
slightly deleterious mutations
in the following surprising
way: by evolving not to repair
mutations. Say a mutation
occurs that if left unrepaired
will be lethal. Now, unless the
process of repair is perfect,
repairing the mutation, while
averting death, may result
in a slightly deleterious mutation instead. Therefore,
Gabriel et ~1.17argue that an
imperfect repair system might
facilitate the accumulation of
slightly deleterious mutations
in an asexual lineage. They
vol.
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REVIEWS
suggest further that while imperfect repair would be benTable 2. Weakened or refuted claims of ancient asexuality
eficial for the individual that
Taxonomic affiliation
Putative ancient clone
Refs
Evidence against
carries it out, a lineage of asexuals that imperfectly repairs
Gastrotricha
Chaetonotoidea
40
sexual phase discovered
DNA would become extinct,
Mollusca: Prosobranchia
Thiaridae
42
sexual spp. discovered
Mollusca: Prosobranchia
Thiara
44
sexual populations discovered
whereas a lineage of asexuals
Mollusca: Prosobranchia
Thiara tuberculata
45
sexual populations discovered
that did not attempt to reArthropoda: Homoptera
Tramini
35
sexual population discovered
pair mutations, while suffering
Arthropoda: Coleoptera
Naupactus leucoloma
group
47
sexual populations discovered
more deaths in each generChordata: Lissamphibia
Ambystoma hybrids
49
nuclear replacement
ation, would reduce the accumulation of mutations in the
longer term. Lynch etal.19have
proposed that animal mitochondria are examples of such a
associated lepiotaceous fungi appears to have been clonally
system in action. Of course, if males usually have much
propagated since the origin of the higher attine ants, and that
higher germ-line genomic mutation rates than females (as
fossils of ants from Dominican amber indicate that the clade
appears to be the case in mammals20),then asexuals may, in of higher attines is at least 25 million years old. However,
any case, face substantially lower mutation pressures than
most claims of antiquity are based on molecular clocks33.
sexual conspecifics.
But convincing support for the most important comAnother way that asexuals could reduce the cost of ponent of a claim of ancient asexuality-- primitive asexuality
asexuality is to increase the mutation rate in particular parts
- is hardest to come by. In most cases, the best arguments
of the genome where mutation is more likely to be beneficial.
that can be made are that no males, or any other evidence of
Although this sounds rather far-fetched at present, prelimisexuality, have ever been recorded. Sceptics reply that furnary models have shown that selection can favour the evoluther study will reveal evidence of sex6; this has happened in
tion of what appear to be mutational hotspots in bacteriazl,
a number of instances (Table 2).
and some evidence for mutational hotspots does exi@. Some
Some lines of evidence can corroborate a claim of ancient
authors have gone further, to suggest that bacteria are able
asexuality. For example, if meiosis has truly been absent for
to direct their mutations23, but this idea remains controvera long time, the chromosome structure, and other structures
sia124.Because the average mutation rate per genome per
associated with meiosis, should degenerate. Karyotypes of
DNAreplication appears to be the same (10-S) for organisms
aphids of the genus Truma show structural heterozygosity51:
with different genome sizes (such that organisms with large
chromosomes are often impossible to sort into pairs, and in
genomes have a lower average mutation rate per base pair),
some cases the ‘diploid’chromosome number is odd - for
Drake24has suggested that there may be an optimal, non-zero
example, 2n =17 or 2n =19 in some races of T. troglodytes.
mutation rate. Note that if the mutation rate per genome per
Likewise, if males have been absent for a sufficient length of
DNAreplication is indeed 10-3, and if the number of replitime, proteins used in spermatogenesis should not be funccations per generation is small, sex should not be necessary
tional (L. Hurst, pers. commun.). But far more compelling
under the mutation-load-reduction hypothesis.
data may be on the way. Meselson has developed a new
method, based on the expected evolution of the nuclear
Detecting ancient asexuals
genome in the absence of meiosis, that has the potential to
In recent years, a number of authors have claimed to have
provide strong positive evidence of ancient asexuality.
identified ancient asexual lineages (Table 1). A claim that a
group of asexual organisms is anciently asexual can be broThe Meselson Method
ken into three components: that the group is descended from
The idea behind the Meselson Method is simple. The main
a common ancestral species (i.e. monophyletic); that it is
genetic consequence of reproducing apomictically (or vegancient; and that it is primitively asexual -that is, asexuality
etatively) is that heterozygosity is preserved rather than
was a characteristic of the ancestral species and one that has
reduced in each generation. Ifapomixis continues, mutations
been preserved without any sexual interludes. A refutation
-neutral mutations in particular-will accumulate and hetercl
of any one of these components would mean that a lineage
zygosity will increase indefinitely. Therefore, an apomictic
cannot be considered to be anciently asexual.
individual that is descended from an ancient apomictic linSupport for monophyly is relatively easy to accumulate:
eage should show extremely high levels of DNA sequence
an analysis of morphological characters, or any others used
heterozygosity, especially at neutral sites.
in systematics, is sufficient. Support for antiquity is somewhat
The argument can be taken further. Imagine an apomictic
more difficult. The first problem is definitional? how old is
lineage that is founded by a single diploid individual. Now
ancient? Sometimes, the only case for antiquity is the extent
consider a gene with two neutral polymorphic alleles of diversification. For example, the Rotifer class Bdelloidea
A and B - within this founding individual. By definition,
comprises four orders, 18 genera and 363 specie@. Some
apomixis has two consequences. First, recombination does
asexual mite clades comprise two families; for instance, the
not occur within the genome of any individual. Thus as a linclade Nematalycidae + Proteonematalycidae has five genera
eage persists through time, A and B accumulate mutations
and 15speciess. Astronger case can be made if the age of the
independently of each other and consequently diverge from
lineage can be quantified. Three methods have been used to
each other: they should be more diverged in every individual
estimate ages: biogeography, the fossil record and molecular
in every descendant generation. Second, recombination does
not occur between the genomes of different individuals.
clocks. Farrar27argues that gametophytes of the Vitturiuand
Trichomanes ferns have been reproducing vegetatively for
Thus, each individual is essentially the founder of a new,
at least 10 million years in North America on the grounds that
evolutionarily independent sublineage; each of these subclimatic conditions there have been unsuitable for sporolineages will also accumulate mutations independently, and
phyte growth since the Miocene. Chapela et al.28 argue, in will diverge from all other sublineages. This means that the
part from phylogenetic evidence, that the ‘Gl’clade of antdivergence of A alleles from B alleles dates back to before
TREE uol. II,
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1996
Refs
41
43,44
43
43
46
48
50
43
REVIEWS
the origin of the apomictic lineage; the divergence of an A
allele in sublineage 1 from the A allele in sublineage 2, however, dates back only to the divergence of these two sublineages, and so on. All these intra-A divergences will be less
than the divergence, found in every individual, between A
and B. The origin of apomixis can, in principle, be dated. To
illustrate, in an ancient apomictic lineage, relationships between alleles in different sublineages should be as shown in
Fig. 1 (compare with Fig. 2). Thus, if a clade of organisms is
truly anciently asexual, we expect the following. First, in as
far as two alleles of the same gene within a single individual
can be recognized as such, they will be extremely heterozygous. Second, divergences between alleles of the same
individual will be greater than the divergences of alleles
between some lineages. Third, the gene copies descended
from the two ancestral alleles, A and B, will have the same
phylogenetic history of branching among sublineages, just
as if they were different loci instead of different alleles. In
contrast, if a group is sexual, we do not necessarily expect
any divergence of A-like alleles within an individual to be
able to tell us the age of the group.
In practice, the method may be difficult to apply. A ‘negative’ result does not necessarily mean that outcrossing has
occurred. For example, a number of complications -such as
gene conversion or other forms of mitotic recombination, a
decay in chromosome structure, or a change in copy number made possible by the lack of meiosis-may obscure the
expected patterns. However, the method, by exploiting the
peculiarities of the evolution of an asexual genome, offers
the best hope for shedding light on the persistence of ancient
asexuality.
The usual suspects
Sofar, no results using the Meselson Method have been
published. In this section, therefore, we will briefly review the
existing evidence for what may be the three most compelling
examples of ancient asexuality (all of which are small, nonmarine aquatic invertebrates): bdelloid rotifers, darwinulid
ostracods, and parthenogenetic brine shrimp (Fig. 3).
Even without evidence from the Meselson Method, the
case for bdelloids being real ancient asexuals seems strong.
First, the bdelloids make up a taxonomic class within which
no males, nor any other evidence of sex, have ever been recorded; this is the highest taxonomic rank assigned to a putative ancient asexual lineage (see Table 1). Second, the Bdelloidea show extensive morphological diversity, indicated by
the ordinal rank given to major bdelloid sublineages and by
the large number of recorded specie9, suggesting that the
bdelloids have been around for millions of years.
Fig. 3. Left: brine shrimp (lo-15
44
A good case can also be made for ancient asexuality in the
ostracod family Darwinulidae. Asexual ostracod lineages are
abundant, but they tend to be of recent originss; for reasons
that are mysterious, the darwinulids seem to be a glaring exception to this rule32.There are 27 extant species of darwinulids (26 in the genus Durwinuluand one in the genus Microdurwinula),with no males known from any of them. This alone
y\
Lineage
3, allele 6
Fig. 1. Expected allele phylogeny for a single-copy nuclear gene within
a completely apomictic or vegetative (i.e. non-meiotic) diploid clade.
(Y: origin of asexuality. B: divergence of lineage 1 from lineages 2 and 3.
y: divergence of lineage 2 from lineage 3. The six terminal ‘taxa’ are the
alleles recovered from three individuals, one each from lineages 1, 2
and 3. The divergence of the two allele lineages, A and B. dates back
to before the origin of asexuality. (Specifically, the divergence dates to
the ‘coalescence’ in the ancestral sexual population of the two alleles
present in the individual that founded the asexual lineage - expected
to be about 2N generations prior to the origin of the asexual lineage,
where N is the population size of the ancestral sexual populatiorP.)
Note that each allele lineage independently reflects the divergences of
lineages 1, 2 and 3.
Lineage
1, allele 6
Lineage
1, allele A
Fig. 2. Expected allele phylogeny for a single-copy nuclear gene within
a sexual diploid clade. (Y: divergence of lineage 1 from lineages 2 and 3.
B: divergence of lineage 2 from lineage 3. The six terminal ‘taxa’ are the
alleles recovered from three individuals, one each from lineages 1, 2
and 3. Relationships between these three organismal lineages are the
same as shown in Fig. 1. Note that in the case of sexuals, the two alleles within each individual are usually expected to have a relatively
recent common ancestor (about 2Ngenerations ago52) and that within
each individual there may be no difference between the two alleles.
mm). Middle: ostracod (l-3 mm). Right: bdelloid rotifer (0.1-0.5
mm). Illustrations by Judy Wearing-Wilde.
TREE
uol. II,
no. 2 February
I.996
REVIE
would qualify the family as putatively ancient. But Darwinulidae is unique among putative ancient asexual lineages in
having a long and rich fossil record: Dunvinul~ are found
from the Carboniferous to the Holocene. What is more, ostracods show sexual dimorphism in their shells that should
make it possible to detect males even when fossilized; putative males are seen in deposits from the Cretaceous that are
between 70 and 90 million years old, but no males have been
found in more recent deposits32. Darwinulidae may offer a
unique opportunity for palaeontological study of the longterm evolution of asexual lineages.
A third lineage, parthenogenetic brine shrimp, is not as
diverse as the bdelloids or the darwinulids but is still remarkable because of the age of 30-40 million years that has
been claimed for it based on mitochondrial DNAsequence
divergence33.Parthenogenetic brine shrimp comprise a clade
that is currently ranked as a single species, Artemia purthenogenetiaW4. High genetic diversity within this clade is
matched by variation in life history, ploidy and other character@. Even the mode of parthenogenesis varies: diploid lineages are automictic and polyploid lineages are apomictic54.
Unlike bdelloids and darwinulids, which live in freshwater,
A. parthenogenetica lives in hypersaline environments that
are biotically depauperate54. This led Perez et ~1.33to suggest
that escape from biotic interactions has enabled A. parthenogentica to persist as an asexual lineage.
ws
Maynard Smith, J. (1986) Contemplating life without sex, Nafure
324,300-301
Suomalainen, E., Suara, A. and Lokki, J. (1987) Cytologyand Eoolution
in Parthenogenesis, CRC Press
Hurst, L.D.,Hamilton, W.D. and Ladle, R.J. (1992) Covert sex, Trends
Ecol. Eool. 7, 144-145
Ladle, R.J., Johnstone, R.A.and Judson, O.P. (1993) Coevolutionary
dynamics of sex In a metapopulation: escaping the Red Queen,
Proc.R. Sot. London Ser. B 253,155-160
Hamilton, W.D. (1980) Sex versus non-sex versus parasite, Oikos
35,282-290
Tooby, J. (1982) Pathogens, polymorphism, and the evolution of
sex, J Theor. Biol. 97,557-576
Ghiselin, M.T. (1974) The Economy of Nature and the Evolution of
Sex, University of California Press
Judson, O.P. (1995) Preserving genes: a model of the
maintenance of genetic variation in a metapopulation under
frequency-dependent selection, Cenet. Res. 65,175-191
12 Muller, H.J. (1964) The relation of recombination to mutational
advance, Mutat Res. 1, 2-9
I3 Gabriel, W. and Wagner, C.P. (1988) Parthenogenetic populations
can remain stable in spite of high mutation rate and random drift,
Natutwissenschaften
75,204-205
I4 Wagner, G.P. and Gabriel, W. (1990) Quantitative variation in flnite
parthenogenetic populations: what stops Mitller’sratchet in the
absence of recombination? Evolution 44,715-731
15 Mogie, M. and Ford, H. (1988) Sexual and asexual Taraxacum
species, Biol. J. Linn. Sot. 35, 155-168
16 Kondrashov, AS. (1994) Miiller’sratchet under epistatic selection,
Genetics 136,1469-1473
Conclusions
Ancient asexuals, if they exist, may hold the key to understanding why sex is maintained in so many populations. On
the face of it, if mutations are a problem encountered
by all organisms, then the persistence of even a few ancient
asexual lineages is peculiar. The pressures on asexuals to
develop ways to control mutation are probably stronger
than on sexuals, which can reduce mutations through sex
and recombination. Further, any asexual individual that
managed to reduce the cost of mutation would be favoured
by selection. However, controlling mutations may be difficult, which may explain why there are not many ancient
asexuals; but mutation, once controlled, is a problem
solved, whereas parasites are a problem that never goes
away. Thus, in our view, organisms reverting to asexuality
may have to overcome a mutational depression that may be
large, but not necessarily insurmountable. Once more conclusive evidence has been gathered to establish that one
or more lineages are truly anciently asexual, experiments
will be needed to see whether such lineages have mechanisms to reduce the effects of mutation or to escape from
parasitism.
Acknowledgements
We thank Matt Meselson, David Welch, Bill Hamilton,
Alan Grafen, Bill Birky, Tim Anderson,
Laurence Hurst,
Judy Wearing-Wilde,
Austin Burt and the Internet.
This work was supported
by grants from the Fulbright
Commission
and the National Science Foundation (O.P.J.)
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Recent advancesin understanding
of the
evolutionand maintenanceof sex
Laurence D. Hurst and Joel R. Peck
S
ex remains an enigma within
The evolution of sex has been the focus
enables the efficient removal of
a mystery. It is baffling for
of considerable attention during recent
deleterious genes. This review will
reasons other than the fact
years. There is some consensus that the
largely be restricted to considerthat, in a typical anisogamous
solution to the mystery is that sex either
ation of these mainstream theories
species with no male investment in
enables the creation and spread of
of sex.
young, a female could have twice
advantageous traits (possibly parasite
Included within the first catas many grandchildren were she
resistance) or helps to purge the genome
egory is a general morass of theasexual’. For example, it is curious
of deleterious mutations. Recent
ories (many of which have yet to be
that if one examines the phylogenexperimental work has allowed testing
formally modelled) that suppose
etic distribution of sex, one finds
of some of the assumptions underlying
that sex is something to do with
that it seems to be quite the oppothe theoretical models, most particularly
evading parasites (for references
site of what one would predict with
whether interactions between genes are
see Refs 2,4,5). These theories are
knowledge of the costs: in poten- synergistic and whether the mutation rate
unusual in so far as they are spetially isogamous groups (in which
is adequately high. However, although a
cific about the sorts of genes that
both sexes invest in offspring and
variety of theories point out advantages
are under selection (those affecthence where the costs of sex are
to sex, most of them predict that a little
ing parasite resistance) and do not
much reduced) the frequency of
sex and recombination can go a long
assume that the selective value of
asexuality seems higher than in
way towards improving the fitness of
an allele is an intrinsic feature of
anisogamous groups, where a much
a population, and it remains unclear
that allele (i.e. what may be an adgreater cost of sex is suffered. If
why obligate sex is so common.
vantageous allele at one moment
sex is so great, then surely those
may become deleterious when paraorganisms with a low cost should
sites have coevolved). Models inLaurence Hurst is at the Dept of Genetics, Downing
do it all the more frequently!
corporating both parasite effects
Street, Cambridge, UK CB2 3EH; Joel Peck is at the
As has been the history of this
and deleterious mutations provide
School of Biological Sciences, The University of
debate for many years now, most
(as might be expected) strong adSussex, Falmer, Brighton, UK BN19QG.
of the work on the evolution of sex
vantages to sex6.
is theoretical, and the past 20years
Despite our focus on the two
have seen a veritable bloom of
categories of theories specified
ideas and subsequent modifications of these. In general,
above, it is important to recognize that there is a variety of
however, from over 20 theories on sex* only two broad
other ideas, many of which may deserve more attention
classes seem to predominated. These are (1) that sex enables
than they are currently receiving. For example, meiosis seems
the spread/creation of advantageous traits, and (2) that sex
to be important in resetting developmental programs and,
46
0 1996,Elsevier Science Ltd
TREE vol.
II,
no. 2 February
1996