What Can Asexual Lineage Age Tell Us About the Maintenance of Sex? Maurine Neiman,A Stephanie Meirmans,B and Patrick G

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 aDepartment of Biology and the Roy J. Carver Center for Comparative Genomics, University of Iowa, Iowa City, Iowa, USA bCentre for the Study of the Sciences and the Humanities, University of Bergen, Bergen, Norway cLaboratoire d’Ecologie Alpine, Universite´ 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 line- not a successful long-term strategy relative to ages is traditionally considered to be “twiggy,” sex (Maynard Smith 1978; Lynch & Gabriel meaning that asexual lineages are short-lived 1983; Hurst et al. 1992; Normark & Lanteri relative to sexual lineages (Weismann 1889; 1998; Burt 2000; Rice 2002). Williams 1975, pp. 162–167; Maynard Smith The ubiquity of sexual reproduction runs 1978, pp. 51–54, 1986; Bell 1982; Avise 1994; counter to the notion that sex faces substantial Normark & Lanteri 1998; Burt 2000; Rice and immediate costs relative to asexual repro- 2002; Simon et al. 2002; Schurko & Logsdon duction (Maynard Smith 1971, 1978; Williams 2008). This pattern implies that asexuality is 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 fo- Address for correspondence: Maurine Neiman, Department of Biology, cusofalargebodyoftheoreticalandem- University of Iowa, Iowa City, IA 52242. Voice: 319-384-1814; fax: 319- 335-1069. [email protected] pirical research. However, despite decades of

The Year in Evolutionary Biology 2009: Ann. N.Y. Acad. Sci. 1168: 185–200 (2009). doi: 10.1111/j.1749-6632.2009.04572.x c 2009 New York Academy of Sciences. 185 186 Annals of the New York Academy of Sciences study and a great deal of attention, this ques- lineate patterns, and discuss their implications. tion remains largely unanswered (Butlin 2002; A main goal of our review is to present the Normark et al. 2003; de Visser & Elena 2007; case that the consideration of the biology, ecol- Hadany & Comeron 2008). ogy, and phylogeography of asexual lineages of all ages is an integral component of a comprehensive evaluation of the advantages of sex. Insights from Studying Asexual We also consider whether merely “old” asexu- Lineage Age als can be distinguished from exceptionally old (i.e., ancient) asexuals and whether the distri- The first direct challenge of the assumption bution of asexual lineage ages that we charac- that asexual lineages almost never persist came terize changes assumptions about the phyloge- from two different studies presenting mitochon- netic distribution of asexuality. We discuss all of drial sequence–based evidence for the exis- this in light of the main classes of hypotheses ∼ tence of 5,000,000-year-old asexual salaman- for sex. der lineages (Hedges et al. 1992; Spolsky et al. 1992). These findings raised awareness that asexual lineages may not be the dead-ends they Review of Asexual Lineage were previously assumed to be, and motivated a Age Estimates flurry of similar studies. A few years later, growing evidence for a diverse array of “ancient Methods asexual” lineages was described as a “power- ful challenge to all theories of sex” (Judson & To determine how asexual lineage ages are Normark 1996). Understanding why and how distributed within and across taxa, we reviewed such “evolutionary scandals” (Maynard Smith the scientific literature for studies reporting es- 1978) persist can help to explain why most or- timates of asexual lineage age in eukaryotic ganisms are sexual (Judson & Normark 1996). taxa containing obligately asexual forms. We This perspective has been a primary mo- included some asexual taxa where asexual line- tivation for the considerable recent efforts to ages have been documented but their age has understand the exceptional status of a few an- not been estimated (e.g., the weevil Aramigus cient asexual species, such as the bdelloid ro- and all included plant taxa), with the goal of tifers (e.g., Gladyshev & Meselson 2008; Mark emphasizing that asexual age estimates are still Welch et al. 2008) and darwinulid ostracods needed for many taxa. When more than one (e.g., Schon¨ et al. 1998, Van Doninck et al. estimate of asexual lineage age was published 2003). Considerably less attention has been de- for a given taxon, we used the most recent one. voted to characterizing and understanding the We also determined whether there were sin- body of asexual lineage age estimates that are gle versus multiple origins of asexual lineages now available from dozens of other taxa. This within each taxon, because the rate of asexual evidence, however, could help to solve the prob- lineage origin is likely to be a major determi- lem of sex. As Butlin (2002) pointed out, insights nant of the extent to which sex faces challenges into the mechanisms maintaining sex can come from asexual invaders (Lively & Howard 1994; from comparing empirical estimates of asexual Burt 2000). Finally, to generate a quantitative, lineage age distribution to the theoretical ex- visual depiction of asexual lineage age distri- pectations under different models for sex. A bution across taxa, we plotted the cumulative comprehensive review of these data has never number of taxa in which asexual lineage age been conducted with this in mind. has been estimated versus the logarithm of the Here, we review the body of existing data maximum asexual lineage age most recently on the distribution of asexual lineage ages, de- reported for a given taxon. Neiman et al.: Asexual Lineage Age and the Maintenance of Sex 187

There is an active debate about how to deter- Results and Interpretation mine whether a putatively asexual lineage is actually asexual (Hurst et al. 1992; Judson & Nor- Our survey indicates that the common as- mark 1996; Lunt 2008; Schurko et al. 2009). sumption that asexual taxa are almost al- One issue that comes up repeatedly is that ways short-lived is frequently violated (Table 1, nearly all asexual lineage age estimates (and Fig. 1; see also Butlin 2002 and Normark et al. determination of asexuality itself) rely upon 2003). For example, more than half of the taxa negative evidence, such as failure to find males (56%) were represented by asexual lineages es- or to detect a recent sexual ancestor (Judson & timated to be >500,000 years old. Not surpris- Normark 1996; Little & Hebert 1996; Normark ingly, the famous “evolutionary scandals,” such et al. 2003; Schurko et al. 2009). This means as the bdelloids, are among the oldest asexual that age estimates are subject to downward re- lineages reported. vision as long as there is, for example, poten- Even so, asexual lineages that have been her- tial for an undiscovered close sexual relative alded as being of exceptional antiquity do not (Robertson et al. 2006), functional males (e.g., appear exceptional when considered against Smith et al. 2006), or cryptic sex (Mikheyev the background of asexual lineage ages esti- et al. 2006; Cooper et al. 2007; Thompson mated from a diverse array of animal taxa. In- et al. 2008). Given that this debate remains un- stead, we found that the relationship between resolved, we simply presented asexual lineage the cumulative number of taxa in which asex- ages as currently estimated. ual lineage age has been estimated and the loga- Also, there exist confounding factors that rithm of the maximum asexual lineage age most could influence our review. For one, there is al- recently reported for a given taxon is quite reg- most certainly a publication bias toward papers ular and nearly linear (Fig. 1). This result has at reporting evidence for ancient asexual lineages, least two interesting implications: (1) there is no because “young” asexual lineages are merely obvious point of demarcation between young behaving as predicted. Another certain source and “ancient” asexuals, with the consequence of bias is taxonomy: for example, no reliable that distinguishing potentially exceptional estimates of asexual lineage age are available (and potentially illuminating) ancient line- forplantseventhoughasexualityiscommonin ages from merely “old” asexual lineages is diffi- plant taxa. This is probably due at least in part cult, and (2) the most parsimonious explanation to the complexity of plant reproductive systems of this pattern of asexual lineage distribution and the perceived lack of suitable molecular is that similar types of mechanisms determine tools. In animals, most estimates of asexual line- maximum asexual lineage ages in all taxa. age age have been made using mitochondrial DNA sequences, which are often useful and ap- Phylogenetic Distribution of Asexuals propriate for this type of inference because of their relatively high and relatively constant rate In light of what appears to be a fairly high rel- of molecular evolution. In plants, both chloro- ative frequency of “old” asexual lineages, is the plast and mitochondrial mutation rates are usu- “twiggy” description still apt (also see Schwan- ally too low to be useful at the time scales of der & Crespi 2009)? One argument in favor interest (Wolfe et al. 1987, but see, e.g., Cho of upholding the status quo is that many of the et al. 2004 and Sloan et al. 2008). This is may older (sometimes called “ancient”) asexual line- be a main reason for why most studies of the ages presented in Table 1 are still relatively evolution and distribution of asexual plant line- young when compared with the average age ages have refrained from estimating the age of of a species. For example, primate species have these lineages (e.g., Mes et al. 2002; Paun et al. an average phylogenetic age of about 4 million 2006; Thompson et al. 2008). years and carnivore species have an average age 188 Annals of the New York Academy of Sciences

TABLE 1. Current Estimates of Asexual Lineage Age Across a Diverse Set of Eukaryotic Taxa Age (thousands No. of Taxona Type of years) Originb origins Methodc Reference

Vertebrates Ambystoma Salamander <25 H Single M, P Robertson et al. 2006 Cnemidophorus Lizard <20 H Multiple R Reeder et al. 2002 Cobitis Fish <100–342 H Multiple A, C, M Janko et al. 2003, 2005 Darevskia Lizard ? H Multiple A Fu et al. 2000b Heteronotia Lizard <300 H Multiple A, C, M, N Moritz 1993; Moritz & Heideman 1993 Lacerta Lizard <5–200 H Multiple M Fu et al. 2000a, c Menidia Atherinid fish ? H Multiple R Echelle 1989 Poecilia Poeciliid fish <100 H Multiple R Avise et al. 1991 Poeciliopsis Poeciliid fish <100–150 H Multiple A, R, T Avise et al. 1992; Quattro et al. 1991, 1992a, 1992b Arthropods Aramigus Weevil ? H Multiple M Normark & Lanteri 1998 Artemia Brine shrimp 3,000 H? ? M Baxevanis et al. 2006 Aspidiotus Scale insect 1,000 I? Single M Provencher et al. 2005 Bryobia Phytophagous ? I Multiple M, N Ros et al. 2008 mite Calligrapha Beetle 300–3,100 H Multiple M, N Gomez-Zurita´ et al. 2006 Daphnia Water flea <20–200 C Multiple M Innes & Hebert 1988; Paland et al. 2005 Darwinulidae Ostracod 200,000 ? Single? F Martens et al. 2003 Eucypris Ostracod <250–4,000 S Multiple M Schon¨ et al. 2000 Heterocypris Ostracod <500(Group I); S Multiple A, M Rossi et al. 2007 8,000–13,000 (Group II, III) Oribatida Mite <200,000 ? Multiple F, N Maraun et al. 2003, 2004; Domes et al. 2007; Heethoff et al. 2007; Laumann et al. 2007 Otiorhynchus Weevil ? H Multiple A Tomiuk & Loeschcke 1992 Rhopalosiphum Aphid “Recent” C Multiple M, N Delmotte et al. 2003; Halkett et al. 2008 Timema Stick insect 250–1,500 H, S Multiple M Sandoval et al. 1998; Law & Crespi 2002 Warramaba Grasshopper ? H Multiple A Honeycutt & Wilkinson 1989 Molluscs Campeloma Prosobranch 100–500 H, S Multiple M, N Johnson 2006 snail Lasaea Clam 5,500–7,600 H Multiple A, M O´ Foighil & Smith 1995; Taylor & O´ Foighil 2000 Continued Neiman et al.: Asexual Lineage Age and the Maintenance of Sex 189

TABLE 1. Continued Age (thousands No. of Taxona Type of years) Originb origins Methodc Reference

Potamopyrgus Prosobranch <40–1,000 S Multiple M Neiman & Lively 2004; snail Neiman et al. 2005 Nematodes Meloidogyne Nematode 40,000 H, S Multiple M, N Castagnone-Sereno 2006; but see Lunt 2008 Platyhelminthes Schmidtea Flatworm <500–1,500 H∗, S? Multiple A, M Pongratz et al. 2003 Rotifers Bdelloidea Bdelloid <100,000 ? ? M Mark Welch & rotifer Meselson 2000 Angiosperms Ranunculus Angiosperm ? S Multiple AF Paun et al. 2006 Taraxacum Angiosperm ? H∗, S Multiple AF Mes et al. 2002; Verduijn et al. 2004; Meirmans 2005 To w ns e ndia Angiosperm ? S Multiple AF, MO Thompson et al. 2008 aAll taxa are genera, except Bdelloidea (class), Oribatida (order), and Darwinulidae (family). bC, contagion; H, hybrid; H∗, hybridization between asexual lineages and sexuals; I, infection, usually Wolbachia; S, spontaneous, usually autopolyploidization. cA, 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. of about 5.5 million years (calculated using the 2007; Heethoff et al. 2007), and darwinulid os- data from Fig. 7.5 in Jones et al. 2005). This tracods (e.g., Pinto et al. 2004). Our review sug- ﬁnding suggests that nearly all of even the most gests that the antiquity of these taxa might not “successful” asexual lineages do not succeed on be so unusual; likewise, their observed high tax- the terms of sexual species. onomic diversity may not be unexpected given Tree topology is determined not only their old age. through the age of the asexual lineage but also through the generation of new branches within the original asexual lineage following Old versus “Ancient” Asexual Lineages its origin from sexual ancestors (Nunney 1989, 1999; Schwander & Crespi 2009). The taxo- The bdelloid rotifers (Maynard Smith 1992; nomic diversity within lineages must thus be a Mark Welch & Meselson 2000; Butlin 2002) function of how long it takes for the asexual and to a lesser extent, the darwinulid ostracods clade in its entirety to become extinct, with the (Butlin 2002; Birky 2004; Martens & Schon¨ expectation that older asexual clades would be 2008) and oribatid mites (Domes et al. 2007) are characterized by higher taxonomic diversity. viewed as exceptionally ancient asexual line- High taxonomic diversity within asexual ages. However, as described in the foregoing, clades has been reported for the bdelloid ro- our review of asexual lineage age distribu- tifers (Birky et al. 2005; Fontaneto et al. 2007), tion revealed no obvious break between these oribatid mites (Maraun et al. 2004; Domes et al. 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 ends. We found that a demarcation point at asexual lineages of various age suggests that 500,000 years—surprisingly, in fact, any de- taxa such as the Rotifera and Darwinula merely marcation point—appears entirely arbitrary. occur at the high end of a fairly regular distribution (Fig. 1). This is in contrast to the apriori expectation that these asexual lineages of ap- Implications for the Maintenance parently singular antiquity would stand out in of Sex amuchmoremarkedway. With this pattern in mind, we now turn to What implications do the patterns apparent the question of when an asexual lineage is old in our review of asexual lineage age distribution enough to be considered unusually so (see also have for validation of the various theories for Maynard Smith 1992; Griffiths & Butlin 1995; sex? Butlin (2002) stated that the relevant the- Law & Crespi 2002). There seems to be a vague ory was still too nascent for asexual lineage age consensus that “unusually ancient” could be distributions to be of much use for identifying defined as the persistence of an asexual line- the mechanism(s) underlying the maintenance age much longer than expected under various of sex. Here, we revisit this issue and connect it mechanisms for the maintenance of sex. How- to other relevant empirical evidence. In partic- ever, as we will review in more detail, it has ular, we review theoretical predictions derived proven quite difficult to establish clear predic- from and empirical evidence for the major hy- tions for asexual lineage age distribution. In the potheses for sex, with special attention to the- absence of a better solution, Law and Crespi ory and data relevant to understanding asexual (2002) defined as “ancient” an asexual lineage lineage persistence and distribution. that has persisted for at least 500,000 genera- More than 20 hypotheses for why sexual tions, with the reasoning that this is likely to reproduction should be maintained in natu- be more than long enough for the extinction of ral populations have been suggested (classified lineages that are ultimately evolutionary dead- by Kondrashov 1993; recently reviewed by, Neiman et al.: Asexual Lineage Age and the Maintenance of Sex 191 e.g., de Visser & Elena 2007 and Hadany & is determined by the rate of generation of new Comeron 2008), nearly all of which invoke lineages and their rate of loss through drift. mechanisms that favor sex because asexual line- As Janko et al. (2008) pointed out, this mech- ages quickly go extinct (Nunney 1989, 1999). anism is similar to the mutation–drift equilib- Two main classes of these hypotheses have been rium of the neutral model of molecular evo- recognized (Kondrashov 1993; Hurst & Peck lution (Kimura & Crow 1964). Under such a 1996; de Visser & Elena 2007; Hadany & model of asexual lineage turnover, the main Comeron 2008): “environmental,” or “ecolog- determinant of mean asexual lineage age in a ical,” hypotheses argue that without sex, asex- population is the rate of creation of new lin- ual lineages cannot keep pace with spatial eages. This leads to the prediction that the age or temporal environmental variation, whereas estimates for asexual species with one origin of the “mutational” hypotheses make the case asexuality should be higher than those for asex- that mutation accumulation is inevitable in uals with multiple origins (Janko et al. 2008). the absence of sex and will eventually lead to We performed a simple test of this predic- extinction. tion by using a randomization test to compare the asexual lineage age estimates from single- Neutral Models for Asexual Lineage Age origin versus multiple-origin asexual lineages represented in Table 1, but we did not find a George Williams pointed out that better un- significant effect of origin frequency (one-sided derstanding of the mechanisms favoring sex can P = 0.20; randomization test with 99,999 per- come from considering the predictions gener- mutations). This result suggests that factors that ated by a “neutral” model where asexual line- were not included in this sort of neutral model age fitness does not decline over time, that is, determine asexual lineage age, with the caveat “clonal decay” (Williams 1975, pp. 162–167; that a publication bias favoring papers featuring also see Maynard Smith 1978, pp. 51–54; Burt old asexual lineages may make such an effect 2000; Butlin 2002; Schwander & Crespi 2009). hard to detect. In other words, evidence for clonal decay can come from comparing the observed asexual Mutational Models lineage age distribution to the appropriate neutral distribution. Because the profound costs Muller (1964) was first to suggest that sex of sex mean that it will usually be maintained might persist because asexual lineages can- by selection when sexuals and asexuals coex- not eliminate harmful mutations. This logic ist, a neutral model that can apply to mixed underlies the common assumption that asex- populations must be compared to the expected ual lineages do not persist because of the fit- age distributions under mechanisms that cre- ness cost imposed by a high mutational load, ate advantages for sex via clonal decay (e.g., and it has featured prominently in two ma- Muller’s ratchet) versus those that do not (e.g., jor hypotheses for sex: Muller’s ratchet (Muller Red Queen). Although no such model exists, 1964) and Kondrashov’s deterministic model a model comparing asexual lineage age distri- (Kondrashov 1982, 1988). bution in entirely asexual populations under The formulation of more specific predictions clonal decay versus a neutral scenario has re- for asexual lineage age distribution when muta- cently been published (Janko et al. 2008). tion accumulation is the primary cause of asex- The most basic form of this model consists ual lineage extinction has not proven easy. For of one population of asexuals, with an influx of example, although Lynch and Gabriel (1990) new asexual lineages derived from a related sex- used an analytical approach to predict that ual species. Lineage turnover occurs through a extinction via Muller’s ratchet should occur process of drift, and asexual lineage diversity within several thousand years, they also found 192 Annals of the New York Academy of Sciences that the rate of extinction was very sensitive to asexual weevils (Tomiuk & Loeschcke 1992), the values of several unexplored key mutational Daphnia (Omilian et al. 2006), aphids (Normark parameters. In particular, time to extinction 1999), darwinulid ostracods (Schon¨ et al. 2004), could become extremely long when mutational and in the oribatid mites (Schaefer et al. 2006). effects can vary. This same dependence on The most ancient of all asexual taxa, however, particular properties of the mutation accumu- does not fit this pattern: the rate of molecu- lation process has also been documented in lar evolution in bdelloid rotifers is higher than other theoretical explorations of the mutational that of close sexual relatives and points toward consequences of asexuality (Bell 1988; mutation accumulation in the absence of sex Kondrashov 1988, 1994; Gabriel et al. (Barraclough et al. 2007). 1993; Gabriel and Burger¨ 2000; Gordo & A different sort of mutational clearance has Charlesworth 2000). New data indicate that been ascribed to another peculiarity of the the rate and spectrum of mutations varies bdelloids: their ability to survive in an “anhy- widely among model systems (Lynch et al. drobiotic,” dormant state, and consequently, 2008), meaning that this information is en- a remarkable tolerance to desiccation (Ricci tirely unknown for most nonmodel taxa (also 1987). Gladyshev and Meselson (2008) sug- see Normark et al. 2003; Birky 2004). The gested that the ability to survive in a dormant, same seems to apply to effective population size desiccated state could confer genetic benefits (Lynch 2007), which plays an integral role in that could underlie the long-term persistence mutation accumulation (Ohta & Kimura 1971). of the asexual bdelloids. More specifically, they Thus, although it is a common expectation that argued that desiccation will often cause double- mutation accumulation should often lead to the stranded DNA breaks that are repaired upon rapid extinction of asexual lineages, quantifi- hydration, and thus that bdelloid evolution has able predictions seem hard to make. In fact, been accompanied by relatively frequent DNA the dependence on many parameters suggests breakage and repair. They also proposed that that asexual lineage extinction due to mutation strong selection for homologous DNA repair accumulation should vary highly across taxa— may have maintained bdelloid chromosomes as a picture that would coincide with our findings collinear pairs, which may both facilitate mu- of high variation in asexual lineage age. tational repair and keep transposable elements What does seem to be undisputed is that in check. mutational mechanisms should work quickly enough so that asexual lineages such as the Ecological/Environmental Models bdelloids and ostracods could not have sur- vived for millions upon millions of years without The other prominent class of hypotheses special adaptations to counteract this process for the predominance of sex proposes that it (Judson & Normark 1996). Thus, one reason- can facilitate adaptation to changing environ- able expectation of mutational models is that mental conditions (Fisher 1930; Muller 1932; ancient asexuals should exhibit specific mech- Williams 1975; Jaenike 1978; Hamilton 1980). anisms, such as efficient DNA repair (but see Under these models, advantages for sex may Gabriel et al. 1993 for a different view), that exist when, for example, organisms produce reduce the rate or cost of mutation accumula- many widely dispersed offspring (the aphid– tion (Kondrashov 1995; Hurst & Peck 1996; rotifer model, Williams 1975) or many offspring Schon¨ & Martens 1998, 2003; Schon¨ et al. with limited dispersal capabilities within a di- 1998; Normark et al. 2003; Birky et al. 2005). verse habitat (Tangled Bank, Bell 1982), or There is mixed support for such mechanisms when there is coevolution between virulent par- from asexual taxa. Evidence for a slow rate of asites/pathogens and their host species (Red molecular evolution has been documented in Queen, Jaenike 1978; Hamilton 1980). Neiman et al.: Asexual Lineage Age and the Maintenance of Sex 193

It is possible to establish some expectations Besides parasite-driven processes, other eco- for asexual lineage age under ecologically based logical processes may also have an important mechanisms for sex, though these predictions influence on asexual lineage age. Indirect evi- must remain qualitative in the absence of spe- dence for this possibility comes from the doc- cific estimates of the rate of environmental umentation of spatially distinct distributions of degeneration. For example, theoretical studies young versus old asexual lineages in Timema have shown that the Red Queen is unlikely to stick insects (Law & Crespi 2002). As docu- cause asexual lineage extinction when acting mented by Law and Crespi (2002), an ancient alone (Howard & Lively 1994). More specifi- asexual Timema lineage is confined to the south- cally, when there are multiple asexual lineages, ern end of the genus range, whereas younger the Red Queen generates a form of balancing lineages are more broadly distributed across the selection driven by frequency-dependent selec- northern part of the range. Law and Crespi tion favoring rare lineages (reviewed in Neiman (2002) also found that younger asexual lineages & Koskella 2009). In general, balancing selec- existed near sexuals, whereas the ancient asex- tion is expected to counter the loss of alleles uals were hundreds of kilometers away from via genetic drift and to thus maintain rela- other sexuals. Law and Crespi interpreted this tively high allelic diversity and old alleles. By pattern as possible evidence in support of a role this logic, Red Queen processes have been im- for geographic separation from sexual competi- plicated as providing a potential explanation tors in the persistence of old asexual Timema for high allelic diversity found in vertebrate lineages, and speculated that disturbance linked major histocompatibility complex loci (Lawlor to the Pleistocene glaciation may have provided et al. 1988; Ebert & Hamilton 1996, reviewed a short-term colonization advantage for asex- in Neiman & Koskella 2009) and in plant dis- ual versus sexual lineages in the northern part ease resistance loci (Bergelson et al. 2001). With of the Timema range. specific regard to asexual lineage age, theory suggests that Red Queen dynamics operating Pluralist Models alone are likely to lead to higher asexual diversity (Lively & Howard 1994) and to an increase Most of these theories for sex reviewed here in asexual lineage age (Howard & Lively 1994) can maintain sex only under strict, perhaps bio- compared with the neutral model outlined in logically implausible, conditions. This has been the preceding. a primary motivation for a recent movement to- A potential link between ancient asexual- ward “pluralist” mechanisms in which multiple ity and spatial or temporal escape from nat- mechanisms combine to maintain sex under a ural enemies has been discussed from a the- broader range of parameter space (West et al. oretical perspective (Ladle et al. 1993). This 1999; Meirmans & Neiman 2006). One plural- point has also been made with regard to bdel- ist mechanism that has received much attention loid rotifers, here in the context of desicca- involves interaction between Muller’s ratchet tion tolerance as a possible means of escape and the Red Queen (Howard & Lively 1994), from pressure from desiccation-sensitive ene- in large part because it predicts that asexual mies (Ladle et al. 1993; Gladyshev & Mesel- lineages should become extinct more quickly son 2008). A different means of evading en- (i.e., have lower mean age) when exposed to emy pressure was suggested by Normark et al. a high risk of infection by coevolving, virulent (2003), who proposed that a high mutation parasites (Howard & Lively 1994; Meirmans & rate in genes related to self/non–self recogni- Neiman 2006). tion (e.g., those encoding the major histocom- Indirect evidence for this type of asexual line- patibility complex) could also facilitate ancient age age distribution has been documented in asexuality. natural populations of Potamopyrgus antipodarum, 194 Annals of the New York Academy of Sciences a New Zealand snail. As described in Neiman truly exceptional feature. This line of reasoning et al. (2005), most asexual P.antipodarum lineages could be subject to a straightforward test: taxo- are recently derived from sexual progenitors, nomic diversity within asexual lineages should with the exception of two asexual clades that increase with asexual lineage age. In reality, apparently are more than 500,000 years old. however, the taxonomic difficulties commonly These putatively ancient asexual clades were associated with asexual taxa and the lack of a found in lakes that had a significantly lower commonly accepted species concept for asex- frequency of sexual individuals than lakes with- uals (Richards 2003) will make such a test out the clades, suggesting that the conditions difficult. that favor sex might also result in relatively What can the distribution of asexual lineage rapid extinction of asexual lineages. Moreover, age variation tell us about the mechanisms de- the old clades were never found in lakes known termining asexual lineage age and the mainte- to have high frequencies of individuals infected nanceofsex?Ideally,wecouldcomparethisdis- by virulent, coevolving, trematode parasites. tribution to predictions made from theoretical This pattern is intriguing in light of the body models for sex, thus either providing evidence of theory and empirical evidence suggesting for or against such models (Butlin 2002). Un- that selective pressure exerted by such parasites fortunately, a formal theoretical framework for may provide a substantial advantage to sex in asexual lineage age does not exist. Instead, we this system (e.g., Lively 1987; Dybdahl & Lively have presented some predictions of and empiri- 1998). cal evidence for the major classes of hypotheses that address asexual lineage age via their more specific focus on the maintenance of sex. Conclusions and Perspective First, we used our asexual lineage age data to perform a simple test of the most basic model We found clear evidence for wide variation for asexual lineage age in the absence of “clonal in asexual lineage ages across taxa. Moreover, decay,” which predicts that mean asexual line- the distribution of asexual lineage age was quite age age should be a positive function of the rate regular and did not show a clear demarcation of origin of new asexual lineages but found no between “young” and “ancient” lineages. In- difference in age between taxa with single ver- deed, even the “scandalous” ancient asexual sus multiple origins of asexual lineages. This taxa such as the bdelloid rotifers merely oc- finding could imply that the rate of origin of curred at the far end of this distribution. Taken new lineages is not the primary factor deter- together, these patterns suggest that similar mining age distribution. types of mechanisms may determine asexual We also concluded that the formulation of lineage age across eukaryotic taxa. quantifiable predictions regarding asexual line- Our review also suggests that most of the age age from mutational models for sex is likely older asexual lineages do not reach ages that to be intrinsically difficult because of their de- are comparable to typical species ages in sex- pendence on many parameters that are both uals, consistent with the often observed twiggy hard to estimate and known to vary exten- phylogenetic distribution of asexual taxa (see sively among taxa. We suggested that the taxon- also Maynard Smith 1978). Three of the old- specific nature of mutation can actually result est asexual taxa that have endured as long as in high lineage age variation across taxa, but sexual taxa typically do—the oribatid mites, more extensive theoretical work that could sup- darwinulid ostracods, and bdelloid rotifers— port this suggestion is needed. What seems to also show a high level of taxonomic diversity. be undisputed is that mutational mechanisms We suggest that this attribute might be a di- should work on time scales far below the ap- rect consequence of their old age rather than a parent ages of some very old asexual lineages, Neiman et al.: Asexual Lineage Age and the Maintenance of Sex 195 such as the bdelloid rotifers. There is indeed a further step toward this goal. Moreover, cur- some (mixed) empirical evidence that some of rent theories for sex almost invariably focus on the very old asexual taxa have special adap- extinction rates of asexual lineages. However, tations that could enable them to counteract asexual lineage ages (and, ultimately, the main- mutational deterioration. tenance of sex in mixed systems) will be deter- We pointed out that some ecological mech- mined through the balance between the rate of anisms for the maintenance of sex, such as origin of new asexual lineages and the rate of the Red Queen, should increase asexual line- their extinction (Maynard Smith 1978; Nunney age age relative to that expected under a neu- 1989; Burt 2000). There is both clear empir- tral model. For the Red Queen, this is a con- ical evidence for taxonomic variation in the sequence of the maintenance of old alleles rate of production of new asexual lineages (re- (and thus lineages) expected under negative viewed in Bell 1982; Butlin 2002; Simon et al. frequency–dependent selection. This situation 2002) and theory suggesting that lineage-level changes drastically under a pluralist model selection will favor sexual lineages with a rela- combining Red Queen and Muller’s ratchet, tively low rate of production of asexual mutants where asexual lineage age in a population is ex- (Nunney 1989, 1999). Thus, although our re- pected to depend on the frequency of infection view did not support the idea that origin rates by virulent, coevolving parasites. Thus, a plu- affect asexual lineage ages, more theory and ralist model predicts asexual lineage age vari- empirical work in this area are needed. ation if parasite pressure varies. There is empirical evidence consistent with the existence of such processes in nature. However, other Acknowledgments ecological mechanisms can also be important We thank J. Jokela, C. Lively, and D. Taylor determinants of asexual lineage age and may for discussion of neutral models for asexual lin- result in intraspecific lineage age variation, as eage age distribution, and D. Taylor for com- suggested by other data. ments on an earlier version of the manuscript. In conclusion, the empirical patterns we found are relatively simple, and the most parsimonious explanation for the observed distribu- Conflicts of Interest tion would be the operation of similar types of mechanisms determining asexual lineage age The authors declare no conflicts of interest. across taxa. However, deriving simple, quantifiable, and discriminative predictions from the References theoretical models remains difficult, which is in part due to their dependence on unknown pa- Avise, J. C. (1994). Molecular Markers, Natural History and rameter values. Even so, we believe that focus- Evolution. New York: Chapman & Hall. ing on asexual lineage ages can give important Avise, J. C., Quattro, M., & Vrijenhoek, R. C. (1992). insights into the maintenance of sex. Part of the Molecular clones within organismal clones: mito- solution is the estimation of key parameters of chondrial DNA phylogenies and the evolutionary history of unisexual vertebrates. Evol. Biol., 26, 225– the models for the maintenance of sex to pro- 246. vide more reliable quantitative predictions for Avise, J. C., Trexler, J. C., Travis, J., & Nelson, W. S. lineage age. (1991). Poecilia mexicana is the recent female parent of In addition to estimating key parameters of the unisexual fish P.formosa. Evolution, 45, 1530–1533. the different models for sex, it is important Barraclough, T. G., Fontaneto, D., Ricci, C., & Herniou, E. A. (2007). Evidence for inefficient selection against to have a more solid theoretical framework deleterious mutations in cytochrome oxidase I of regarding asexual lineage age. Our presenta- asexual bdelloid rotifers. Mol. Biol. Evol., 24, 1952– tion of theoretical predictions should provide 1962. 196 Annals of the New York Academy of Sciences

Baxevanis, A. D., Kappas, I., & Abatzopoulos, T.J. (2006). Fisher, R. A. (1930). The Genetical Theory of Natural Selection. Molecular phylogenetics and asexuality in the brine Oxford, UK: Clarendon Press. shrimp Artemia. Mol. Phylogenet. Evol., 40, 724–738. Fontaneto, D., Nerniou, E. A., Boschetti, C., Caprioli, M., Bell, G. (1982). The Masterpiece of Nature. London: Croon Melone, G., Ricci, C., & Barraclough, T. G. (2007). Helm. Independently evolving species in asexual bdelloid Bell, G. (1988). Uniformity and diversity in the evolu- rotifers. PLoS Biol., 5, e87. tion of sex. In R. E. Michod & B. R. Levin (Eds.), Fu, J., MacCulloch, R. D., Murphy, R. W., & Darevsky, The Evolution of Sex (pp. 126–138). Sunderland, MA: I. S. (2000a). Clonal variation in the Caucasian Sinauer. rock lizard Lacerta armeniaca and its origin. Amphibia- Bergelson, J., Kreitman, M., Stahl, E. A., & Tian, D. Reptilia, 21, 83–88. (2001). Evolutionary dynamics of plant R-genes. Sci- Fu, J., MacCulloch, R. D., Murphy,R. W., Darevsky, I. S., ence, 292, 2281–2285. & Tuniyev,B. S. (2000b). Allozyme variation patterns Birky, C. W., Jr. (2004). Bdelloid rotifers revisited. Proc. and multiple hybridization origins: clonal variation Natl. Acad. Sci. USA, 101, 2651–2652. among four sibling parthenogenetic Caucasian rock Birky, C. W., Jr., Wolf, C., Maughan, H., Herbertson, L., lizards. Genetica, 108, 107–112. & Henry, E. (2005). Speciation and selection without Fu, J., Murphy, R. W., & Darevsky, I. S. (2000c). Diver- sex. Hydrobiologia, 546, 29–45. gence of the cytochrome b gene in the Lacerta raddei Burt, A. (2000). Perspective: sex, recombination, and the complex and its parthenogenetic daughter species: efficacy of selection: was Weismann right? Evolution, evidence for recent multiple origins. Copeia, 2000, 54, 337–351. 432–440. Butlin, R. (2002). The costs and benefits of sex: new in- Gabriel, W., & R. Burger.¨ (2000). Fixation of clonal lin- sights from old asexual lineages. Nat. Rev. Genet., 3, eages under Muller’s ratchet. Evolution, 54, 1116– 311–317. 1125. Castagnone-Sereno, P. (2006) Genetic variability and Gabriel, W., Lynch, M., & Burger,¨ R. (1993). Muller’s adaptive evolution in parthenogenetic root-knot ne- ratchet and mutational meltdowns. Evolution, 47, matodes. Heredity, 96, 282–289. 1744–1757. Cho, Y., Mower, J. P., Qiu, Y.-L., & Palmer, J. D. (2004). Gladyshev, E., & Meselson, M. (2008). Extreme resistance Mitochondrial substitution rates are extraordinarily of bdelloid rotifers to ionizing radiation. Proc. Natl. elevated and variable in a genus of flowering plants. Acad. Sci. USA, 105, 5139–5144. Proc. Natl. Acad. Sci. USA, 101, 17741–17746. Gomez-Zurita,´ J., Funk, D. J., & Vogler, A. P. (2006). Cooper, M. A., Adam, R. D., Worobey, M., & Sterling, C. The evolution of unisexuality in Calligrapha leaf bee- R. (2007). Population genetics provides evidence for tles: molecular and ecological insights on multiple recombination in Giardia. Curr. Biol., 17, 1984–1988. origins via interspecific hybridization. Evolution, 60, Delmotte, F., Sabater-Munoz,˜ B., Prunier-Leterme, N., 328–347. Latorre, A., Sunnucks, P., Rispe, C., & Simon, J. C. Gordo, I., & Charlesworth, B. (2000). The degenera- (2003). Phylogenetic evidence for hybrid origins of tion of asexual haploid populations and the speed asexual lineages in an aphid species. Evolution, 57, of Muller’s ratchet. Genetics, 154, 1379–1387. 1291–1303. Griffiths, H. I., & Butlin, R. K. (1995). A timescale for de Visser, J. A. G. M., & Elena, S. F.(2007). The evolution sex versus parthenogenesis: evidence from subfossil of sex: empirical insights into the roles of epistasis ostracods. Proc. R. Soc. Lond. B Biol. Sci., 260, 65–71. and drift. Nat. Rev. Genet., 8, 139–149. Hadany, L., & Comeron, J. M. (2008). Why are sex and re- Domes, K., Norton, R. A., Maraun, M., & Scheu, S. combination so common? Ann. N. Y. Acad. Sci., 1133, (2007). Reevolution of sexuality breaks Dollo’s law. 26–43. Proc. Natl. Acad. Sci. USA, 104, 7139–7144. Halkett, F., Plantegenest, M., Bonhomme, J., & Simon, Dybdahl, M. F., & Lively, C. M. (1998). Host-parasite J. C. (2008). Gene flow between sexual and faculta- coevolution: evidence for rare advantage and time- tively asexual lineages of an aphid species and the lagged selection in a natural population. Evolution, maintenance of reproductive mode variation. Mol. 52, 1057–1066. Ecol., 17, 2998–3007. Ebert, D., & Hamilton, W. D. (1996). Sex against vir- Hamilton, W.D. (1980). Sex vs. non-sex vs. parasite. Oikos, ulence: the coevolution of parasitic diseases. Trends 35, 282–290. Ecol. Evol., 11, 79–82. Hedges, S. B., Bogart, J. P.,& Maxson, L. R. 1992. Ances- Echelle, A. A. (1989). Mitochondrial-DNA diversity and try of unisexual salamanders. Nature, 356, 708–710. the origin of the Menidia clarkshubbsi complex of Heethoff, M., Domes, K., Laumann, M., Maraun, M., unisexual fishes (Atherinidae). Evolution, 43, 984– Norton, R. A., & Scheu, S. (2007). High ge- 993. netic divergences indicate ancient separation of Neiman et al.: Asexual Lineage Age and the Maintenance of Sex 197

parthenogenetic lineages of the oribatid mite Kondrashov, A. S. (1993). Classification of hypotheses on Platynothrus peltifer (Acari, Oribatida). J. Evol. Biol., the advantage of amphimixis. J. Hered., 84, 372–387. 20, 392–402. Kondrashov, A. S. (1994). Muller’s ratchet under epistatic Honeycutt, R. L., & Wilkinson, P. (1989). Electrophoretic selection. Genetics, 136, 1469–1473. variation in the parthenogenetic grasshopper War- Kondrashov, A. S. (1995). Modifiers of mutation— ramba virgo and its sexual relatives. Evolution, 43, 1027– selection balance: general approach and the evolu- 1044. tion of mutation rates. Genet. Res., 66, 53–69. Howard, R. S., & Lively, C. M. (1994). Parasitism, mu- Ladle, R. J., Johnstone, R. A., & Judson, O. P. (1993). Co- tation accumulation, and the maintenance of sex. evolutionary dynamics of sex in a metapopulation: Nature, 367, 554–557. catching the Red Queen. Proc.R.Soc.Lond.BBiol. Hurst, L. D., Hamilton, W. D., & Ladle, R. J. (1992). Sci., 253, 155–160. Covert sex. Trends Ecol. Evol., 7, 144–145. Laumann, M., Norton, R. A., Weigmann, G., Scheu, S., Hurst, L. D., & Peck, J. R. (1996). Recent advances in Maraun, M., & Heethoff, M. (2007). Speciation in understanding the evolution and maintenance of sex. the parthenogenetic mite genus Tectocepheus (Acari, Trends Ecol. Evol., 11, 46–53. Oribatida) as indicated by molecular phylogeny. Pe- Innes, D. J., & Hebert, P. D. N. (1988). The origin and dobiologia, 51, 111–122. genetic basis of obligate parthenogenesis in Daphnia Law, J. H., & Crespi, B. J. (2002). Recent and ancient asex- pulex. Evolution, 42, 1024–1035. uality in Timema walkingsticks. Evolution, 56, 1711– Jaenike, J. (1978). An hypothesis to account for the main- 1717. tenance of sex within populations. Evol. Theor., 3, Lawlor, D. A., Ward, F. E., Ennis, P. D., Jackson, A. P., 191–194. & Parham, P. (1988). HLA-A and B polymorphisms Janko, K., Culling, M. A., Rab,´ P.,& Kotl´ık, P.(2005). Ice predate the divergence of humans and chimpanzees. age cloning—comparison of the Quaternary evolu- Nature, 335, 268–271. tionary histories of sexual and clonal forms of spiny Little, T. J., & Hebert, P. D. N. (1996). Ancient asexuals: loaches (Cobitis; Teleostei) using the analysis of mi- scandal or artifact? Trends Ecol. Evol., 11, 296. tochondrial DNA variation. Mol. Ecol., 14, 2991– Lively, C. M. (1987). Evidence from a New Zealand snail 3004. for the maintenance of sex by parasitism. Nature, 328, Janko, K., Drozd, P., Flegr, J., & Pannell, J. R. (2008). 519–521. Clonal turnover versus clonal decay: a null model Lively, C. M., & Howard, R. S. (1994). Selection by par- for observed patterns of asexual longevity, diversity asites for clonal diversity and mixed mating. Proc. R. and distribution. Evolution, 62, 1264–1270. Soc.Lond.BBiol.Sci., 346, 271–281. Janko, K., Kotlik, P., & Rab,´ P. (2003). Evolutionary his- Lunt, D. H. (2008). Genetic tests of ancient asexuality tory of asexual hybrid loaches (Cobitis: Teleostei) in- in root knot nematodes reveal recent hybrid origins. ferred from phylogenetic analysis of mitochondrial BMC Evol. Biol., 8, 194. DNA variation. J. Evol. Biol., 16, 1280–1287. Lynch, M. (2007). The Origins of Genome Architecture.Sun- Johnson, S. G. (2006). Geographic ranges, population derland, MA: Sinauer Associates. structure, and ages of sexual parthenogenetic snail Lynch, M., & Gabriel, W. (1983). Phenotypic evolution lineages. Evolution, 60, 1417–1426. and parthenogenesis. Am. Nat., 122, 745–764. Jones, K. E., Sechrest, W., & Gittleman, J. L. (2005). Age Lynch, M., & Gabriel, W. (1990). Mutation load and the and area revisited: identifying global patterns and survival of small populations. Evolution, 44, 1725– implications for conservation. In A. Purvis, J. L. Git- 1737. tleman & T. Brooks (Eds.), Phylogeny and Conservation Lynch, M., Sung, W., Moris, K., Coffey, N., Landry, C. (pp. 141–165). Cambridge, UK: Cambridge Univer- R., Dopman, E. B., Dickinson, W. J., Okamoto, K., sity Press. Kulkarni, S., Hartl, D. L., & Thomas, W.K. (2008). A Judson, O. P., & Normark, B. B. 1996. Ancient asexual genome-wide view of the spectrum of spontaneous scandals. Trends Ecol. Evol., 11, A41–A46. mutations in yeast. Proc. Natl. Acad. Sci. USA, 105, Kimura, M., & Crow, J. F. (1964). The number of alleles 9272–9277. that can be maintained in a finite population. Genetics, Maraun, M., Heethoff, M., Scheu, S., Norton, R. A., 49, 725–738. Weigmann, G., & Thomas, R. H. (2003). Radiation Kondrashov, A. S. (1982). Selection against harmful mu- in sexual and parthenogenetic oribatid mites (Ori- tations in large sexual and asexual populations. Genet. batida, Acari) as indicated by genetic divergence of Res., 40, 325–332. closely related species. Exp. Appl. Acarol., 29, 265– Kondrashov, A. S. (1988). Deleterious mutations and the 277. evolution of sexual reproduction. Nature, 336, 435– Maraun, M., Heethoff, M., Schneider, K., Scheu, S., 440. Weigmann, G., Cianciolo, J., Thomas, R. H., & 198 Annals of the New York Academy of Sciences

Norton, R. A. (2004). Molecular phylogeny of orib- Lost Sex: The Evolutionary Biology of Parthenogenesis.Dor- atid mites (Oribatida, Acari): evidence for multiple drecht, the Netherlands: Springer, in press. radiations of parthenogenetic lineages. Exp. Appl. Ac- Neiman, M., Jokela, J., & Lively, C. M. (2005). Variation arol., 33, 183–201. in asexual lineage age in Potamopyrgus antipodarum,a Mark Welch, D. B., Mark Welch, J. L., & Meselson, M. New Zealand snail. Evolution, 59, 1945–1952. (2008). Evidence for degenerate tetraploidy in bdel- Neiman, M., & Lively, C. M. (2004). Pleistocene glacia- loid rotifers. Proc. Natl. Acad. Sci. USA, 105, 5145– tion is implicated in the phylogeographical structure 5149. of Potamopyrgus antipodarum, a New Zealand snail. Mol. Mark Welch, D. B., & Meselson, M. S. (2000). Evidence Ecol., 13, 3085–3098. for the evolution of bdelloid rotifers without sex- Normark, B. B. (1999). Evolution in a putatively an- ual recombination or genetic exchange. Science, 288, cient asexual aphid lineage: recombination and rapid 1211–1215. karyotype change. Evolution, 53, 1458–1469. Martens, K., Rossetti, G., & Home, D. J. (2003). How Normark, B. B., Judson, O. P., & Moran, N. A. (2003). ancient are ancient asexuals? Proc. R. Soc. Lond. B Genomic signatures of ancient asexual lineages. Biol. Biol. Sci., 270, 723–729. J. Linn. Soc. Lond., 79, 69–84. Martens, K., & I. Schon.¨ (2008). Ancient asexuals: dar- Normark, B. B., & Lanteri, A. A. (1998). Incongruence be- winulids not exposed. Nature, 453, 587. tween morphological and mitochondrial-DNA char- Maynard Smith, J. (1971). What use is sex? J. T heor. Biol., acters suggests hybrid origins of parthenogenetic 30, 319–335. weevillineages (Genus Aramigus). Syst. Biol., 47, 475– Maynard Smith, J. (1978). The Evolution of Sex. London: 494. Cambridge University Press. Nunney, L. (1989). The maintenance of sex by group Maynard Smith, J. (1986). Contemplating life without sex. selection. Evolution, 43, 245–257. Nature, 324, 300–301. Nunney, L. (1999). Lineage selection: natural selection for Maynard Smith, J. (1992). Age and the unisexual lineage. long-term beneﬁt. In L. Keller (Ed.), Levels of Selection Nature, 356, 661–662. in Evolution (pp. 238–254). Princeton, NJ: Princeton Meirmans, P. (2005). Ecological and genetic interactions University Press. between diploid sexual and triploid apomictic dan- O´ Foighil, D., & Smith, M. J. (1995). Evolution of asexual- delions. PhD thesis. University of Amsterdam, Ams- ity in the cosmopolitan marine clam Lasaea. Evolution, terdam, the Netherlands. 49, 140–150. Meirmans, S., & Neiman, M. (2006). Methodologies for Ohta, T., & Kimura, M. (1971). On the constancy of the testing a pluralistic model for the maintenance of evolutionary rate of cistrons. J. Mol. Evol., 1, 18– sex. Biol. J. Linn. Soc. Lond., 89, 605–613. 25. Mes, T. H. M., Kuperus, P., Kirschner, J., Stepˇ anek,´ J., Omilian, A. R., Cristescu, M. E. A., Dudycha, J. L., & Storchovˇ a,´ H., Oosterveld, P., & Den Nijs, J. C. Lynch, M. (2006). Ameiotic recombination in asex- M. (2002). Detection of genetically divergent clone ual lineages of Daphnia. Proc.Natl.Acad.Sci.USA, 103, mates in apomictic dandelions. Mol. Ecol., 11, 253– 18638–18643. 265. Paland, S., Colbourne, J. K., & Lynch, M. (2005). Evo- Mikheyev, A. S., Mueller, U. G., & Abbot, P.(2006). Cryp- lutionary history of contagious asexuality in Daphnia tic sex and many-to-one coevolution in the fungus- pulex. Evolution, 59, 800–813. growing ant symbiosis. Proc. Natl. Acad. Sci. USA, 103, Paun, O., Greilhuber, J., Temsch, E. M., & Horandl,¨ E. 10702–10706. (2006). Patterns, sources and ecological implications Moritz, C. (1993). The origin and evolution of partheno- of clonal diversity in apomictic Ranunculus carpaticola genesis in the Heteronotia binoei complex. Genetica, 90, (Ranunculus auricomus complex, Ranunculaceae). Mol. 269–280. Ecol., 15, 897–910 Moritz, C., & Heideman, A. (1993). The origin and Pinto, R. L., Rocha, C. E. F., & Martens, K. (2004). On evolution of parthenogenesis in Heteronotia binoei the genus Penthesilenula Rossetti and Martens, 1998 (Gekkonidae): reciprocal origins and diverse mito- (Crustacea, Ostracoda, Darwinulidae) from (semi-) chondrial DNA in western populations. Syst. Biol., terrestrial habitats in Sao˜ Paulo State (Brazil), with 42, 293–306. the description of a new species. J. Nat. Hist., 38, Muller, H. J. (1932). Some genetic aspects of sex. Am. Nat., 2567–2589. 66, 118–138. Pongratz, N., Storhas, M., Carranza, S., & Michiels, Muller, H. J. (1964). The relation of recombination to N. K. (2003). Phylogeography of competing sex- mutational advance. Mutat. Res., 1, 2–9. ual and parthenogenetic forms of a freshwater ﬂat- Neiman, M., & Koskella, B. (2009). Sex and the Red worm: patterns and explanations. BMC Evol. Biol., 3, Queen.InI.Schon,¨ K. Martens, & P.Van Dijk (Eds.), 23. Neiman et al.: Asexual Lineage Age and the Maintenance of Sex 199

Provencher, L. M., Morse, G. E., Weeks, A. R., & Nor- Schon,¨ I., Butlin, R. K., Griffiths, H. I., & Martens, K. mark, B. B. (2005). Parthenogenesis in the Aspidiotus (2004). Slow molecular evolution in an ancient asex- nerii complex (Hemiptera: Diaspididae): a single ori- ual ostracod. Proceedings of the Royal Society of gin of a worldwide, polyphagous lineage associated London B. Biological Sciences, 265, 235–242. with Cardinium bacteria. Ann. Entomol. Soc. Am., 98, Schon,¨ I., Gandolfi, A., Di Masso, E., Rossi, V.,Griffiths, 629–635. H. I., & Martens, K. (2000). Persistence of asexu- Quattro, J. M., Avise, J. C., & Vrijenhoek, R. C. (1991). ality through mixed reproduction in Eucypris virens Molecular evidence for multiple origins of hybrido- (Crustacea, Ostracoda). Heredity, 84, 161–169. genetic fish clones (Poeciliidae: Poeciliopsis). Genetics, Schon,¨ I., & Martens, K. (1998). DNA repair in ancient 127, 391–398. asexuals—a new solution to an old problem? J. Nat. Quattro, J. M., Avise, J. C., & Vrijenhoek, R. C. (1992a). Hist., 32, 943–949. An ancient clonal lineage in the fish genus Poeciliop- Schon,¨ I., & Martens, K. (2003). No slave to sex. Proc. R. sis (Atheriniformes: Poeciliidae). Proc. Natl. Acad. Sci. Soc.Lond.BBiol.Sci., 270, 827–833. USA, 89, 348–352. Schurko, A. M., & Logsdon, J. M., Jr. (2008). Using a Quattro, J. M., Avise, J. C., & Vrijenhoek, R. C. (1992b). meiosis detection toolkit to investigate ancient asex- Mode of origin and sources of genotypic diversity ual “scandals” and the evolution of sex. Bioessays, 30, in triploid gynogenetic fish clones (Poeciliopsis: Poecil- 579–589. iopsis). Genetics, 130, 621–628. Schurko, A. M., Neiman, M., & Logsdon, J. M., Jr. (2009). Reeder, T.W., Cole, C. J., & Dessauer, H. C. (2002). Phy- Signs of sex: what we know and how we know it. logenetic relationships of whiptail lizards of the genus Trends Ecol. Evol., 24, 208–217. Cnemidophorus (Squamata: Teiidae): a test of mono- Schwander, T., & Crespi, B. J. (2009). Twigs on the tree phyly, reevaluation of karyotypic evolution, and re- of life? Neutral and selective models for integrating view of hybrid origins. Am.Mus.Novit., 3365, 1–61. macroevolutionary patterns with microevolutionary Ricci, C. (1987). Ecology of bdelloids: how to be success- processes in the analysis of asexuality. Molecular Ecol- ful. Hydrobiologia, 147, 117–127. ogy, 18, 28–42. Rice, W. R. (2002). Experimental tests of the adaptive Simon, J.-C., Rispe, C., & Sunnucks, P. (2002). Ecology significance of sexual reproduction. Nat. Rev. Genet., and evolution of sex in aphids. Trends Ecol. Evol., 17, 3, 241–250. 34–39. Richards, A. J. (2003). Apomixis in flowering plants: an Sloan, D. B., Barr, C. M., Olson, M. S., Keller, S. R., overview. Philos. Trans. R. Soc. Lond. B Biol. Sci., 358, & Taylor, D. R. (2008). Evolutionary rate varia- 1085–1093. tion at multiple levels of biological organization in Robertson, A. V., Ramsden, C., Niedzwiecki, J., Fu, J., & plant mitochondrial DNA. Mol. Biol. Evol., 25, 243– Bogart, J. P. (2006). An unexpected recent ancestor 246. of unisexual Ambystoma. Mol. Ecol., 15, 3339–3351. Smith, R. J., Kamiya, T., & Horne, D. J. (2006). Living Ros, V.I. D., Breeuwer, J. A. J., & Menken, S. B. J. (2008). males of the ‘ancient asexual’ Darwinulidae (Ostra- Origins of asexuality in Bryobia mites (Acari: Tetrany- coda: Crustacea). Proc. R. Soc. Lond. B Biol. Sci., 273, chidae). BMC Evol. Biol., 8, 153. 1569–1578. Rossi, V., Gandolfi, A., Baraldi, F., Bellavere, C., & Spolsky, C. M., Phillips, C. A., & Uzzell, T. (1992). An- Menozzi, P. (2007). Phylogenetic relationships of co- tiquity of clonal salamander lineages revealed by existing Heterocypris (Crustacea, Ostracoda) lineages mitochondrial-DNA. Nature, 356, 706–708. with different reproductive modes from Lampedusa Taylor, D. J., & O´ Foighil, D. (2000). Transglobal com- Island (Italy). Mol. Phylogenet. Evol., 44, 1273–1283. parisons of nuclear and mitochondrial genetic struc- Sandoval, C., Carmean, D. A., & Crespi, B. J. (1998). ture in a marine polyploid clam (Lasaea, Lasaeidae). Molecular phylogenetics of sexual and partheno- Heredity, 84, 321–330. genetic Timema walking-sticks. Proc. R. Soc. Lond. B Thompson, S. L., Choe, G., Ritland, K., & Whitton, Biol. Sci., 265, 589–595. J. (2008). Cryptic sex within male-sterile polyploid Schaefer, I., Domes, K., Heethoff, M., Schneider, K., populations of the Easter daisy, Townsendia hookeri. Schon,¨ I., Norton, R. A., Scheu, S., & Maraun, Int. J. Plant Sci., 169, 183–193. M. (2006). No evidence for the “Meselson effect” Tomiuk, J., & Loeschcke, V.(1992). Evolution of partheno- in parthenogenetic oribatid mites (Oribatida, Acari). genesis in the Otiorhynchus scaber complex. Heredity, 68, J. Evol. Biol., 19, 184–193. 391–398. Schon,¨ I., Butlin, R. K., Griffiths, H. I., & Martens, K. Van Doninck, K., Schon,¨ I., Maes, F., De Bruyn, L., (1998). Slow molecular evolution in an ancient asex- & Martens, K. (2003). Ecological strategies in the ual ostracod. Proc. R. Soc. Lond. B Biol. Sci., 265, 235– ancient asexual animal group Darwinulidae (Crus- 242. tacea, Ostracoda). Freshw. Biol., 48, 1285–1294. 200 Annals of the New York Academy of Sciences

Verduijn, M. H., Van Dijk, P. J., & Van Damme, J. M. West, S. A., Lively, C. M., & Read, A. F. (1999). A plu- M. (2004). The role of tetraploids in the sexual– ralistic approach to sex and recombination. J. Evol. asexual cycle in dandelions (Taraxacum). Heredity, 93, Biol., 12, 1003–1012. 390–398. Williams, G. C. (1975). Sex and Evolution.Princeton,NJ: Weismann, A. (1889). The signiﬁcance of sexual repro- Princeton University Press. duction in the theory of natural selection. In E. B. Wolfe, K. H., Li, W.-H., & Sharp, P. M. (1987). Rates Poulton, S. Schonland¨ & A. E. Shipley (Eds.), Essays of nucleotide substitution vary greatly among plant upon Heredity and Kindred Biological Problems (Vol. I, pp. mitochondrial, chloroplast and nuclear DNAs. Proc. 255–332). Oxford: Clarendon Press. Natl. Acad. Sci. USA, 84, 9054–9058.