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THE YEAR IN EVOLUTIONARY BIOLOGY 2009
What Can Asexual Lineage Age Tell Us about
the Maintenance of Sex?
Maurine Neiman,a Stephanie Meirmans,b
and Patrick G. Meirmansc
a
Department of Biology and the Roy J. Carver Center for Comparative Genomics,
University of Iowa, Iowa City, Iowa, USA
b
Centre for the Study of the Sciences and the Humanities, University of Bergen,
Bergen, Norway
c
Laboratoire d’Ecologie Alpine, Université Joseph Fourier, Grenoble, France
Sexual reproduction is both extremely costly and extremely common relative to asexuality, indicating that it must confer profound benefits. This in turn points to major
disadvantages of asexual reproduction, which is usually given as an explanation for why
almost all asexual lineages are apparently quite short-lived. However, a growing body
of evidence suggests that some asexual lineages are actually quite old. Insight into why
sex is so common may come from understanding why asexual lineages persist in some
places or taxa but not others. Here, we review the distribution of asexual lineage ages
estimated from a diverse array of taxa, and we discuss our results in light of the main
mutational and environmental hypotheses for sex. Along with strengthening the case
for wide variation in asexual lineage age and the existence of many old asexual taxa, we
also found that the distribution of asexual lineage age estimates follows a surprisingly
regular distribution, to the extent that asexual taxa viewed as “scandalously” ancient
merely fall on the high end of this distribution. We interpret this result to mean that
similar mechanisms may determine asexual lineage age across eukaryotic taxa. We also
derive some qualitative predictions for asexual lineage age under different theories for
sex and discuss empirical evidence for these predictions. Ultimately, we were limited
in the extent to which we could use these data to make inferences about the maintenance of sex by the absence of both clear theoretical expectations and estimates of key
parameters.
Key words: sex; asexual; parthenogenetic; ancient asexual; lineage age; scandal
The phylogenetic distribution of asexual lineages is traditionally considered to be “twiggy,”
meaning that asexual lineages are short-lived
relative to sexual lineages (Weismann 1889;
Williams 1975, pp. 162–167; Maynard Smith
1978, pp. 51–54, 1986; Bell 1982; Avise 1994;
Normark & Lanteri 1998; Burt 2000; Rice
2002; Simon et al. 2002; Schurko & Logsdon
2008). This pattern implies that asexuality is
Address for correspondence: Maurine Neiman, Department of Biology,
University of Iowa, Iowa City, IA 52242. Voice: 319-384-1814; fax: 319335-1069. [email protected]
not a successful long-term strategy relative to
sex (Maynard Smith 1978; Lynch & Gabriel
1983; Hurst et al. 1992; Normark & Lanteri
1998; Burt 2000; Rice 2002).
The ubiquity of sexual reproduction runs
counter to the notion that sex faces substantial
and immediate costs relative to asexual reproduction (Maynard Smith 1971, 1978; Williams
1975). These costs are so profound that understanding why sex is so common has been
termed the “queen of questions” (Bell 1982)
in evolutionary biology and has been the focus of a large body of theoretical and empirical research. However, despite decades of
The Year in Evolutionary Biology 2009: Ann. N.Y. Acad. Sci. 1168: 185–200 (2009).
c 2009 New York Academy of Sciences.
doi: 10.1111/j.1749-6632.2009.04572.x 185
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Annals of the New York Academy of Sciences
study and a great deal of attention, this question remains largely unanswered (Butlin 2002;
Normark et al. 2003; de Visser & Elena 2007;
Hadany & Comeron 2008).
Insights from Studying Asexual
Lineage Age
The first direct challenge of the assumption
that asexual lineages almost never persist came
from two different studies presenting mitochondrial sequence–based evidence for the existence of ∼5,000,000-year-old asexual salamander lineages (Hedges et al. 1992; Spolsky et al.
1992). These findings raised awareness that
asexual lineages may not be the dead-ends they
were previously assumed to be, and motivated a
flurry of similar studies. A few years later, growing evidence for a diverse array of “ancient
asexual” lineages was described as a “powerful challenge to all theories of sex” (Judson &
Normark 1996). Understanding why and how
such “evolutionary scandals” (Maynard Smith
1978) persist can help to explain why most organisms are sexual (Judson & Normark 1996).
This perspective has been a primary motivation for the considerable recent efforts to
understand the exceptional status of a few ancient asexual species, such as the bdelloid rotifers (e.g., Gladyshev & Meselson 2008; Mark
Welch et al. 2008) and darwinulid ostracods
(e.g., Schön et al. 1998, Van Doninck et al.
2003). Considerably less attention has been devoted to characterizing and understanding the
body of asexual lineage age estimates that are
now available from dozens of other taxa. This
evidence, however, could help to solve the problem of sex. As Butlin (2002) pointed out, insights
into the mechanisms maintaining sex can come
from comparing empirical estimates of asexual
lineage age distribution to the theoretical expectations under different models for sex. A
comprehensive review of these data has never
been conducted with this in mind.
Here, we review the body of existing data
on the distribution of asexual lineage ages, de-
lineate patterns, and discuss their implications.
A main goal of our review is to present the
case that the consideration of the biology, ecology, and phylogeography of asexual lineages of
all ages is an integral component of a comprehensive evaluation of the advantages of sex.
We also consider whether merely “old” asexuals can be distinguished from exceptionally old
(i.e., ancient) asexuals and whether the distribution of asexual lineage ages that we characterize changes assumptions about the phylogenetic distribution of asexuality. We discuss all of
this in light of the main classes of hypotheses
for sex.
Review of Asexual Lineage
Age Estimates
Methods
To determine how asexual lineage ages are
distributed within and across taxa, we reviewed
the scientific literature for studies reporting estimates of asexual lineage age in eukaryotic
taxa containing obligately asexual forms. We
included some asexual taxa where asexual lineages have been documented but their age has
not been estimated (e.g., the weevil Aramigus
and all included plant taxa), with the goal of
emphasizing that asexual age estimates are still
needed for many taxa. When more than one
estimate of asexual lineage age was published
for a given taxon, we used the most recent one.
We also determined whether there were single versus multiple origins of asexual lineages
within each taxon, because the rate of asexual
lineage origin is likely to be a major determinant of the extent to which sex faces challenges
from asexual invaders (Lively & Howard 1994;
Burt 2000). Finally, to generate a quantitative,
visual depiction of asexual lineage age distribution across taxa, we plotted the cumulative
number of taxa in which asexual lineage age
has been estimated versus the logarithm of the
maximum asexual lineage age most recently
reported for a given taxon.
Neiman et al.: Asexual Lineage Age and the Maintenance of Sex
There is an active debate about how to determine whether a putatively asexual lineage is actually asexual (Hurst et al. 1992; Judson & Normark 1996; Lunt 2008; Schurko et al. 2009).
One issue that comes up repeatedly is that
nearly all asexual lineage age estimates (and
determination of asexuality itself) rely upon
negative evidence, such as failure to find males
or to detect a recent sexual ancestor (Judson &
Normark 1996; Little & Hebert 1996; Normark
et al. 2003; Schurko et al. 2009). This means
that age estimates are subject to downward revision as long as there is, for example, potential for an undiscovered close sexual relative
(Robertson et al. 2006), functional males (e.g.,
Smith et al. 2006), or cryptic sex (Mikheyev
et al. 2006; Cooper et al. 2007; Thompson
et al. 2008). Given that this debate remains unresolved, we simply presented asexual lineage
ages as currently estimated.
Also, there exist confounding factors that
could influence our review. For one, there is almost certainly a publication bias toward papers
reporting evidence for ancient asexual lineages,
because “young” asexual lineages are merely
behaving as predicted. Another certain source
of bias is taxonomy: for example, no reliable
estimates of asexual lineage age are available
for plants even though asexuality is common in
plant taxa. This is probably due at least in part
to the complexity of plant reproductive systems
and the perceived lack of suitable molecular
tools. In animals, most estimates of asexual lineage age have been made using mitochondrial
DNA sequences, which are often useful and appropriate for this type of inference because of
their relatively high and relatively constant rate
of molecular evolution. In plants, both chloroplast and mitochondrial mutation rates are usually too low to be useful at the time scales of
interest (Wolfe et al. 1987, but see, e.g., Cho
et al. 2004 and Sloan et al. 2008). This is may
be a main reason for why most studies of the
evolution and distribution of asexual plant lineages have refrained from estimating the age of
these lineages (e.g., Mes et al. 2002; Paun et al.
2006; Thompson et al. 2008).
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Results and Interpretation
Our survey indicates that the common assumption that asexual taxa are almost always short-lived is frequently violated (Table 1,
Fig. 1; see also Butlin 2002 and Normark et al.
2003). For example, more than half of the taxa
(56%) were represented by asexual lineages estimated to be >500,000 years old. Not surprisingly, the famous “evolutionary scandals,” such
as the bdelloids, are among the oldest asexual
lineages reported.
Even so, asexual lineages that have been heralded as being of exceptional antiquity do not
appear exceptional when considered against
the background of asexual lineage ages estimated from a diverse array of animal taxa. Instead, we found that the relationship between
the cumulative number of taxa in which asexual lineage age has been estimated and the logarithm of the maximum asexual lineage age most
recently reported for a given taxon is quite regular and nearly linear (Fig. 1). This result has at
least two interesting implications: (1) there is no
obvious point of demarcation between young
and “ancient” asexuals, with the consequence
that distinguishing potentially exceptional
(and potentially illuminating) ancient lineages from merely “old” asexual lineages is difficult, and (2) the most parsimonious explanation
of this pattern of asexual lineage distribution
is that similar types of mechanisms determine
maximum asexual lineage ages in all taxa.
Phylogenetic Distribution of Asexuals
In light of what appears to be a fairly high relative frequency of “old” asexual lineages, is the
“twiggy” description still apt (also see Schwander & Crespi 2009)? One argument in favor
of upholding the status quo is that many of the
older (sometimes called “ancient”) asexual lineages presented in Table 1 are still relatively
young when compared with the average age
of a species. For example, primate species have
an average phylogenetic age of about 4 million
years and carnivore species have an average age
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TABLE 1. Current Estimates of Asexual Lineage Age Across a Diverse Set of Eukaryotic Taxa
Age
(thousands
of years)
Originb
No. of
origins
Methodc
Reference
<25
<20
<100–342
?
<300
H
H
H
H
H
Single
Multiple
Multiple
Multiple
Multiple
M, P
R
A, C, M
A
A, C, M, N
<5–200
?
<100
<100–150
H
H
H
H
Multiple
Multiple
Multiple
Multiple
M
R
R
A, R, T
Robertson et al. 2006
Reeder et al. 2002
Janko et al. 2003, 2005
Fu et al. 2000b
Moritz 1993; Moritz &
Heideman 1993
Fu et al. 2000a, c
Echelle 1989
Avise et al. 1991
Avise et al. 1992;
Quattro et al. 1991,
1992a, 1992b
?
H
Multiple
M
H?
I?
I
?
Single
Multiple
M
M
M, N
Calligrapha
Brine shrimp
3,000
Scale insect
1,000
Phytophagous
?
mite
Beetle
300–3,100
H
Multiple
M, N
Daphnia
Water flea
<20–200
C
Multiple
M
Ostracod
200,000
Ostracod
<250–4,000
Ostracod <500(Group I);
8,000–13,000
(Group II, III)
Mite
<200,000
?
S
S
Single?
Multiple
Multiple
F
M
A, M
?
Multiple
F, N
Otiorhynchus
Weevil
?
H
Multiple
A
Rhopalosiphum
Aphid
“Recent”
C
Multiple
M, N
Timema
Stick insect
250–1,500
H, S
Multiple
M
Warramaba
Grasshopper
H
Multiple
A
H, S
Multiple
M, N
Johnson 2006
H
Multiple
A, M
Ó Foighil & Smith
1995; Taylor & Ó
Foighil 2000
Taxona
Type
Vertebrates
Ambystoma
Cnemidophorus
Cobitis
Darevskia
Heteronotia
Salamander
Lizard
Fish
Lizard
Lizard
Lizard
Atherinid fish
Poeciliid fish
Poeciliid fish
Lacerta
Menidia
Poecilia
Poeciliopsis
Arthropods
Aramigus
Artemia
Aspidiotus
Bryobia
Darwinulidae
Eucypris
Heterocypris
Oribatida
Molluscs
Campeloma
Lasaea
Weevil
?
Prosobranch
100–500
snail
Clam
5,500–7,600
Normark & Lanteri
1998
Baxevanis et al. 2006
Provencher et al. 2005
Ros et al. 2008
Gómez-Zurita et al.
2006
Innes & Hebert 1988;
Paland et al. 2005
Martens et al. 2003
Schön et al. 2000
Rossi et al. 2007
Maraun et al. 2003,
2004; Domes et al.
2007; Heethoff et al.
2007; Laumann
et al. 2007
Tomiuk & Loeschcke
1992
Delmotte et al. 2003;
Halkett et al. 2008
Sandoval et al. 1998;
Law & Crespi 2002
Honeycutt &
Wilkinson 1989
Continued
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Neiman et al.: Asexual Lineage Age and the Maintenance of Sex
TABLE 1. Continued
Taxona
Type
Potamopyrgus
Prosobranch
snail
Nematodes
Meloidogyne
Platyhelminthes
Schmidtea
Rotifers
Bdelloidea
Age
(thousands
of years)
Originb
<40–1,000
S
Multiple
M
Neiman & Lively 2004;
Neiman et al. 2005
H, S
Multiple
M, N
Castagnone-Sereno
2006; but see Lunt
2008
H∗ , S?
Multiple
A, M
Pongratz et al. 2003
?
?
M
Mark Welch &
Meselson 2000
Paun et al. 2006
Mes et al. 2002;
Verduijn et al. 2004;
Meirmans 2005
Thompson et al. 2008
Nematode
40,000
Flatworm
<500–1,500
Bdelloid
rotifer
<100,000
No. of
origins
Methodc
Angiosperms
Ranunculus
Taraxacum
Angiosperm
Angiosperm
?
?
S
H∗ , S
Multiple
Multiple
AF
AF
Townsendia
Angiosperm
?
S
Multiple
AF, MO
Reference
a
All taxa are genera, except Bdelloidea (class), Oribatida (order), and Darwinulidae (family).
C, contagion; H, hybrid; H∗ , hybridization between asexual lineages and sexuals; I, infection, usually Wolbachia;
S, spontaneous, usually autopolyploidization.
c
A, allozyme; AF, amplified fragment length polymorphism; C, chromosome structure; F, fossil; M, mtDNA sequence; MO, morphology; N, nuclear sequence; P, phylogeography/biogeography; R, restriction fragment length
polymorphism; T, tissue grafts.
b
of about 5.5 million years (calculated using the
data from Fig. 7.5 in Jones et al. 2005). This
finding suggests that nearly all of even the most
“successful” asexual lineages do not succeed on
the terms of sexual species.
Tree topology is determined not only
through the age of the asexual lineage but
also through the generation of new branches
within the original asexual lineage following
its origin from sexual ancestors (Nunney 1989,
1999; Schwander & Crespi 2009). The taxonomic diversity within lineages must thus be a
function of how long it takes for the asexual
clade in its entirety to become extinct, with the
expectation that older asexual clades would be
characterized by higher taxonomic diversity.
High taxonomic diversity within asexual
clades has been reported for the bdelloid rotifers (Birky et al. 2005; Fontaneto et al. 2007),
oribatid mites (Maraun et al. 2004; Domes et al.
2007; Heethoff et al. 2007), and darwinulid ostracods (e.g., Pinto et al. 2004). Our review suggests that the antiquity of these taxa might not
be so unusual; likewise, their observed high taxonomic diversity may not be unexpected given
their old age.
Old versus “Ancient” Asexual Lineages
The bdelloid rotifers (Maynard Smith 1992;
Mark Welch & Meselson 2000; Butlin 2002)
and to a lesser extent, the darwinulid ostracods
(Butlin 2002; Birky 2004; Martens & Schön
2008) and oribatid mites (Domes et al. 2007) are
viewed as exceptionally ancient asexual lineages. However, as described in the foregoing,
our review of asexual lineage age distribution revealed no obvious break between these
taxa and all other asexual taxa. Instead, our
190
Annals of the New York Academy of Sciences
Figure 1. The cumulative number of taxa in which asexual lineage age has been estimated
as a function of the logarithm of the maximum asexual lineage age most recently reported for
a given taxon (Fig. 1). All data are taken from Table 1. Age estimates for the “scandalous”
Bdelloidea, Darwinulidae, and Oribatida are circled.
comparison of the frequency distribution of
asexual lineages of various age suggests that
taxa such as the Rotifera and Darwinula merely
occur at the high end of a fairly regular distribution (Fig. 1). This is in contrast to the a priori
expectation that these asexual lineages of apparently singular antiquity would stand out in
a much more marked way.
With this pattern in mind, we now turn to
the question of when an asexual lineage is old
enough to be considered unusually so (see also
Maynard Smith 1992; Griffiths & Butlin 1995;
Law & Crespi 2002). There seems to be a vague
consensus that “unusually ancient” could be
defined as the persistence of an asexual lineage much longer than expected under various
mechanisms for the maintenance of sex. However, as we will review in more detail, it has
proven quite difficult to establish clear predictions for asexual lineage age distribution. In the
absence of a better solution, Law and Crespi
(2002) defined as “ancient” an asexual lineage
that has persisted for at least 500,000 generations, with the reasoning that this is likely to
be more than long enough for the extinction of
lineages that are ultimately evolutionary dead-
ends. We found that a demarcation point at
500,000 years—surprisingly, in fact, any demarcation point—appears entirely arbitrary.
Implications for the Maintenance
of Sex
What implications do the patterns apparent
in our review of asexual lineage age distribution
have for validation of the various theories for
sex? Butlin (2002) stated that the relevant theory was still too nascent for asexual lineage age
distributions to be of much use for identifying
the mechanism(s) underlying the maintenance
of sex. Here, we revisit this issue and connect it
to other relevant empirical evidence. In particular, we review theoretical predictions derived
from and empirical evidence for the major hypotheses for sex, with special attention to theory and data relevant to understanding asexual
lineage persistence and distribution.
More than 20 hypotheses for why sexual
reproduction should be maintained in natural populations have been suggested (classified
by Kondrashov 1993; recently reviewed by,
191
Neiman et al.: Asexual Lineage Age and the Maintenance of Sex
e.g., de Visser & Elena 2007 and Hadany &
Comeron 2008), nearly all of which invoke
mechanisms that favor sex because asexual lineages quickly go extinct (Nunney 1989, 1999).
Two main classes of these hypotheses have been
recognized (Kondrashov 1993; Hurst & Peck
1996; de Visser & Elena 2007; Hadany &
Comeron 2008): “environmental,” or “ecological,” hypotheses argue that without sex, asexual lineages cannot keep pace with spatial
or temporal environmental variation, whereas
the “mutational” hypotheses make the case
that mutation accumulation is inevitable in
the absence of sex and will eventually lead to
extinction.
Neutral Models for Asexual Lineage Age
George Williams pointed out that better understanding of the mechanisms favoring sex can
come from considering the predictions generated by a “neutral” model where asexual lineage fitness does not decline over time, that is,
“clonal decay” (Williams 1975, pp. 162–167;
also see Maynard Smith 1978, pp. 51–54; Burt
2000; Butlin 2002; Schwander & Crespi 2009).
In other words, evidence for clonal decay can
come from comparing the observed asexual
lineage age distribution to the appropriate neutral distribution. Because the profound costs
of sex mean that it will usually be maintained
by selection when sexuals and asexuals coexist, a neutral model that can apply to mixed
populations must be compared to the expected
age distributions under mechanisms that create advantages for sex via clonal decay (e.g.,
Muller’s ratchet) versus those that do not (e.g.,
Red Queen). Although no such model exists,
a model comparing asexual lineage age distribution in entirely asexual populations under
clonal decay versus a neutral scenario has recently been published (Janko et al. 2008).
The most basic form of this model consists
of one population of asexuals, with an influx of
new asexual lineages derived from a related sexual species. Lineage turnover occurs through a
process of drift, and asexual lineage diversity
is determined by the rate of generation of new
lineages and their rate of loss through drift.
As Janko et al. (2008) pointed out, this mechanism is similar to the mutation–drift equilibrium of the neutral model of molecular evolution (Kimura & Crow 1964). Under such a
model of asexual lineage turnover, the main
determinant of mean asexual lineage age in a
population is the rate of creation of new lineages. This leads to the prediction that the age
estimates for asexual species with one origin of
asexuality should be higher than those for asexuals with multiple origins (Janko et al. 2008).
We performed a simple test of this prediction by using a randomization test to compare
the asexual lineage age estimates from singleorigin versus multiple-origin asexual lineages
represented in Table 1, but we did not find a
significant effect of origin frequency (one-sided
P = 0.20; randomization test with 99,999 permutations). This result suggests that factors that
were not included in this sort of neutral model
determine asexual lineage age, with the caveat
that a publication bias favoring papers featuring
old asexual lineages may make such an effect
hard to detect.
Mutational Models
Muller (1964) was first to suggest that sex
might persist because asexual lineages cannot eliminate harmful mutations. This logic
underlies the common assumption that asexual lineages do not persist because of the fitness cost imposed by a high mutational load,
and it has featured prominently in two major hypotheses for sex: Muller’s ratchet (Muller
1964) and Kondrashov’s deterministic model
(Kondrashov 1982, 1988).
The formulation of more specific predictions
for asexual lineage age distribution when mutation accumulation is the primary cause of asexual lineage extinction has not proven easy. For
example, although Lynch and Gabriel (1990)
used an analytical approach to predict that
extinction via Muller’s ratchet should occur
within several thousand years, they also found
192
that the rate of extinction was very sensitive to
the values of several unexplored key mutational
parameters. In particular, time to extinction
could become extremely long when mutational
effects can vary. This same dependence on
particular properties of the mutation accumulation process has also been documented in
other theoretical explorations of the mutational
consequences of asexuality (Bell 1988;
Kondrashov 1988, 1994; Gabriel et al.
1993; Gabriel and Bürger 2000; Gordo &
Charlesworth 2000). New data indicate that
the rate and spectrum of mutations varies
widely among model systems (Lynch et al.
2008), meaning that this information is entirely unknown for most nonmodel taxa (also
see Normark et al. 2003; Birky 2004). The
same seems to apply to effective population size
(Lynch 2007), which plays an integral role in
mutation accumulation (Ohta & Kimura 1971).
Thus, although it is a common expectation that
mutation accumulation should often lead to the
rapid extinction of asexual lineages, quantifiable predictions seem hard to make. In fact,
the dependence on many parameters suggests
that asexual lineage extinction due to mutation
accumulation should vary highly across taxa—
a picture that would coincide with our findings
of high variation in asexual lineage age.
What does seem to be undisputed is that
mutational mechanisms should work quickly
enough so that asexual lineages such as the
bdelloids and ostracods could not have survived for millions upon millions of years without
special adaptations to counteract this process
(Judson & Normark 1996). Thus, one reasonable expectation of mutational models is that
ancient asexuals should exhibit specific mechanisms, such as efficient DNA repair (but see
Gabriel et al. 1993 for a different view), that
reduce the rate or cost of mutation accumulation (Kondrashov 1995; Hurst & Peck 1996;
Schön & Martens 1998, 2003; Schön et al.
1998; Normark et al. 2003; Birky et al. 2005).
There is mixed support for such mechanisms
from asexual taxa. Evidence for a slow rate of
molecular evolution has been documented in
Annals of the New York Academy of Sciences
asexual weevils (Tomiuk & Loeschcke 1992),
Daphnia (Omilian et al. 2006), aphids (Normark
1999), darwinulid ostracods (Schön et al. 2004),
and in the oribatid mites (Schaefer et al. 2006).
The most ancient of all asexual taxa, however,
does not fit this pattern: the rate of molecular evolution in bdelloid rotifers is higher than
that of close sexual relatives and points toward
mutation accumulation in the absence of sex
(Barraclough et al. 2007).
A different sort of mutational clearance has
been ascribed to another peculiarity of the
bdelloids: their ability to survive in an “anhydrobiotic,” dormant state, and consequently,
a remarkable tolerance to desiccation (Ricci
1987). Gladyshev and Meselson (2008) suggested that the ability to survive in a dormant,
desiccated state could confer genetic benefits
that could underlie the long-term persistence
of the asexual bdelloids. More specifically, they
argued that desiccation will often cause doublestranded DNA breaks that are repaired upon
hydration, and thus that bdelloid evolution has
been accompanied by relatively frequent DNA
breakage and repair. They also proposed that
strong selection for homologous DNA repair
may have maintained bdelloid chromosomes as
collinear pairs, which may both facilitate mutational repair and keep transposable elements
in check.
Ecological/Environmental Models
The other prominent class of hypotheses
for the predominance of sex proposes that it
can facilitate adaptation to changing environmental conditions (Fisher 1930; Muller 1932;
Williams 1975; Jaenike 1978; Hamilton 1980).
Under these models, advantages for sex may
exist when, for example, organisms produce
many widely dispersed offspring (the aphid–
rotifer model, Williams 1975) or many offspring
with limited dispersal capabilities within a diverse habitat (Tangled Bank, Bell 1982), or
when there is coevolution between virulent parasites/pathogens and their host species (Red
Queen, Jaenike 1978; Hamilton 1980).
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Neiman et al.: Asexual Lineage Age and the Maintenance of Sex
It is possible to establish some expectations
for asexual lineage age under ecologically based
mechanisms for sex, though these predictions
must remain qualitative in the absence of specific estimates of the rate of environmental
degeneration. For example, theoretical studies
have shown that the Red Queen is unlikely to
cause asexual lineage extinction when acting
alone (Howard & Lively 1994). More specifically, when there are multiple asexual lineages,
the Red Queen generates a form of balancing
selection driven by frequency-dependent selection favoring rare lineages (reviewed in Neiman
& Koskella 2009). In general, balancing selection is expected to counter the loss of alleles
via genetic drift and to thus maintain relatively high allelic diversity and old alleles. By
this logic, Red Queen processes have been implicated as providing a potential explanation
for high allelic diversity found in vertebrate
major histocompatibility complex loci (Lawlor
et al. 1988; Ebert & Hamilton 1996, reviewed
in Neiman & Koskella 2009) and in plant disease resistance loci (Bergelson et al. 2001). With
specific regard to asexual lineage age, theory
suggests that Red Queen dynamics operating
alone are likely to lead to higher asexual diversity (Lively & Howard 1994) and to an increase
in asexual lineage age (Howard & Lively 1994)
compared with the neutral model outlined in
the preceding.
A potential link between ancient asexuality and spatial or temporal escape from natural enemies has been discussed from a theoretical perspective (Ladle et al. 1993). This
point has also been made with regard to bdelloid rotifers, here in the context of desiccation tolerance as a possible means of escape
from pressure from desiccation-sensitive enemies (Ladle et al. 1993; Gladyshev & Meselson 2008). A different means of evading enemy pressure was suggested by Normark et al.
(2003), who proposed that a high mutation
rate in genes related to self/non–self recognition (e.g., those encoding the major histocompatibility complex) could also facilitate ancient
asexuality.
Besides parasite-driven processes, other ecological processes may also have an important
influence on asexual lineage age. Indirect evidence for this possibility comes from the documentation of spatially distinct distributions of
young versus old asexual lineages in Timema
stick insects (Law & Crespi 2002). As documented by Law and Crespi (2002), an ancient
asexual Timema lineage is confined to the southern end of the genus range, whereas younger
lineages are more broadly distributed across the
northern part of the range. Law and Crespi
(2002) also found that younger asexual lineages
existed near sexuals, whereas the ancient asexuals were hundreds of kilometers away from
other sexuals. Law and Crespi interpreted this
pattern as possible evidence in support of a role
for geographic separation from sexual competitors in the persistence of old asexual Timema
lineages, and speculated that disturbance linked
to the Pleistocene glaciation may have provided
a short-term colonization advantage for asexual versus sexual lineages in the northern part
of the Timema range.
Pluralist Models
Most of these theories for sex reviewed here
can maintain sex only under strict, perhaps biologically implausible, conditions. This has been
a primary motivation for a recent movement toward “pluralist” mechanisms in which multiple
mechanisms combine to maintain sex under a
broader range of parameter space (West et al.
1999; Meirmans & Neiman 2006). One pluralist mechanism that has received much attention
involves interaction between Muller’s ratchet
and the Red Queen (Howard & Lively 1994),
in large part because it predicts that asexual
lineages should become extinct more quickly
(i.e., have lower mean age) when exposed to
a high risk of infection by coevolving, virulent
parasites (Howard & Lively 1994; Meirmans &
Neiman 2006).
Indirect evidence for this type of asexual lineage age distribution has been documented in
natural populations of Potamopyrgus antipodarum,
194
Annals of the New York Academy of Sciences
a New Zealand snail. As described in Neiman
et al. (2005), most asexual P. antipodarum lineages
are recently derived from sexual progenitors,
with the exception of two asexual clades that
apparently are more than 500,000 years old.
These putatively ancient asexual clades were
found in lakes that had a significantly lower
frequency of sexual individuals than lakes without the clades, suggesting that the conditions
that favor sex might also result in relatively
rapid extinction of asexual lineages. Moreover,
the old clades were never found in lakes known
to have high frequencies of individuals infected
by virulent, coevolving, trematode parasites.
This pattern is intriguing in light of the body
of theory and empirical evidence suggesting
that selective pressure exerted by such parasites
may provide a substantial advantage to sex in
this system (e.g., Lively 1987; Dybdahl & Lively
1998).
Conclusions and Perspective
We found clear evidence for wide variation
in asexual lineage ages across taxa. Moreover,
the distribution of asexual lineage age was quite
regular and did not show a clear demarcation
between “young” and “ancient” lineages. Indeed, even the “scandalous” ancient asexual
taxa such as the bdelloid rotifers merely occurred at the far end of this distribution. Taken
together, these patterns suggest that similar
types of mechanisms may determine asexual
lineage age across eukaryotic taxa.
Our review also suggests that most of the
older asexual lineages do not reach ages that
are comparable to typical species ages in sexuals, consistent with the often observed twiggy
phylogenetic distribution of asexual taxa (see
also Maynard Smith 1978). Three of the oldest asexual taxa that have endured as long as
sexual taxa typically do—the oribatid mites,
darwinulid ostracods, and bdelloid rotifers—
also show a high level of taxonomic diversity.
We suggest that this attribute might be a direct consequence of their old age rather than a
truly exceptional feature. This line of reasoning
could be subject to a straightforward test: taxonomic diversity within asexual lineages should
increase with asexual lineage age. In reality,
however, the taxonomic difficulties commonly
associated with asexual taxa and the lack of a
commonly accepted species concept for asexuals (Richards 2003) will make such a test
difficult.
What can the distribution of asexual lineage
age variation tell us about the mechanisms determining asexual lineage age and the maintenance of sex? Ideally, we could compare this distribution to predictions made from theoretical
models for sex, thus either providing evidence
for or against such models (Butlin 2002). Unfortunately, a formal theoretical framework for
asexual lineage age does not exist. Instead, we
have presented some predictions of and empirical evidence for the major classes of hypotheses
that address asexual lineage age via their more
specific focus on the maintenance of sex.
First, we used our asexual lineage age data to
perform a simple test of the most basic model
for asexual lineage age in the absence of “clonal
decay,” which predicts that mean asexual lineage age should be a positive function of the rate
of origin of new asexual lineages but found no
difference in age between taxa with single versus multiple origins of asexual lineages. This
finding could imply that the rate of origin of
new lineages is not the primary factor determining age distribution.
We also concluded that the formulation of
quantifiable predictions regarding asexual lineage age from mutational models for sex is likely
to be intrinsically difficult because of their dependence on many parameters that are both
hard to estimate and known to vary extensively among taxa. We suggested that the taxonspecific nature of mutation can actually result
in high lineage age variation across taxa, but
more extensive theoretical work that could support this suggestion is needed. What seems to
be undisputed is that mutational mechanisms
should work on time scales far below the apparent ages of some very old asexual lineages,
195
Neiman et al.: Asexual Lineage Age and the Maintenance of Sex
such as the bdelloid rotifers. There is indeed
some (mixed) empirical evidence that some of
the very old asexual taxa have special adaptations that could enable them to counteract
mutational deterioration.
We pointed out that some ecological mechanisms for the maintenance of sex, such as
the Red Queen, should increase asexual lineage age relative to that expected under a neutral model. For the Red Queen, this is a consequence of the maintenance of old alleles
(and thus lineages) expected under negative
frequency–dependent selection. This situation
changes drastically under a pluralist model
combining Red Queen and Muller’s ratchet,
where asexual lineage age in a population is expected to depend on the frequency of infection
by virulent, coevolving parasites. Thus, a pluralist model predicts asexual lineage age variation if parasite pressure varies. There is empirical evidence consistent with the existence
of such processes in nature. However, other
ecological mechanisms can also be important
determinants of asexual lineage age and may
result in intraspecific lineage age variation, as
suggested by other data.
In conclusion, the empirical patterns we
found are relatively simple, and the most parsimonious explanation for the observed distribution would be the operation of similar types of
mechanisms determining asexual lineage age
across taxa. However, deriving simple, quantifiable, and discriminative predictions from the
theoretical models remains difficult, which is in
part due to their dependence on unknown parameter values. Even so, we believe that focusing on asexual lineage ages can give important
insights into the maintenance of sex. Part of the
solution is the estimation of key parameters of
the models for the maintenance of sex to provide more reliable quantitative predictions for
lineage age.
In addition to estimating key parameters of
the different models for sex, it is important
to have a more solid theoretical framework
regarding asexual lineage age. Our presentation of theoretical predictions should provide
a further step toward this goal. Moreover, current theories for sex almost invariably focus on
extinction rates of asexual lineages. However,
asexual lineage ages (and, ultimately, the maintenance of sex in mixed systems) will be determined through the balance between the rate of
origin of new asexual lineages and the rate of
their extinction (Maynard Smith 1978; Nunney
1989; Burt 2000). There is both clear empirical evidence for taxonomic variation in the
rate of production of new asexual lineages (reviewed in Bell 1982; Butlin 2002; Simon et al.
2002) and theory suggesting that lineage-level
selection will favor sexual lineages with a relatively low rate of production of asexual mutants
(Nunney 1989, 1999). Thus, although our review did not support the idea that origin rates
affect asexual lineage ages, more theory and
empirical work in this area are needed.
Acknowledgments
We thank J. Jokela, C. Lively, and D. Taylor
for discussion of neutral models for asexual lineage age distribution, and D. Taylor for comments on an earlier version of the manuscript.
Conflicts of Interest
The authors declare no conflicts of interest.
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