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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 185 186 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). 187 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 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 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 189 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). 193 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). 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