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Animal Clones and Diversity Are natural clones generalists or specialists? Robert C. Vrijenhoek A sexual reproduction, or cloning, occurs naturally in most animal phyla. Indeed, alternation between sexual and asexual phases of the life cycle is relatively common in some invertebrate taxa. However, obligately (i.e., strictly) asexual "species" are rare, comprising little more than 1 in every 1000 of the named animal species (White 1978). Biologists study these exceptions to the "rule of sex" for the same reasons that medical scientists probe disorders and diseases to define the limits of human health. Identifying the conditions in which asexual lineages prosper or fail provides -a window through which biologists can view the adaptive significance of genetic diversity and sex. The lessons to be learned from natural clones are particularly relevant as an era begins in which the artificial cloning of mammals, and potentially humans, is no longer a fantasy. To an evolutionary biologist, sex is meiotic recombination· and outcrossing, which together create genetically diverse offspring that interact uniquely with the environment in each new generation. Meiotic sex originated in our single-celled protist ancestors, and except for the evolution of distinct male and female gametes (i.e., small motile sperm Robert C. Vrijenhoek (e-mail: vrijen@ ahab.rutgcrs.edu) is director of the Center for Theoretical and Applied Genetics at Rutgers University, New Brunswick, NJ 08903-0231. His interests are evolution, population genetics, conservation, and marine biology. © 1998 American Institutc of Biological Scicnces. August 1998 Studies of animal clones provide insight into the ecological benefits of genetic variability and large eggs), the basic sexual mechanism has changed little in the evolution of multicellular plants and animals. Nevertheless, the origins of sex and factors that maintain such a complex and costly process have been hotly debated among evolutionary biologists (Williams 1975, Maynard Smith 1978, Bell 1982, Michod 1995). Perhaps clues to the benefits of sex can be learned by studying organisms that have abandoned this process. Obligately asexual lineages have arisen naturally in most animal taxa (with the exception of birds and mammals), and clones flourish in certain environments. Nevertheless, individual clones appear to be evolutionary dead ends with limited adaptive potential. Few obligately asexual taxa (with the notable exception of bdelloid rotifers) have diversified to the point at which a taxonomist would name new species and genera (White 1978). A low rate of diversification, coupled with a high rate of extinction, may explain why there are so few asexual species (Stanley 1975). On the tree of life, asexual animals represent little more than a few twigs at the tips of bountiful branches that are fundamentally sexual. Apart from mutations, asexual progeny are genetically identical to their mothers. An asexual population may be composed of a single clone whose genotype is essentially constant across generations. At the opposite extreme, random sexual matings produce a nearly unlimited array of genotypes and phenotypes that differ in each generation. Most natural populations lie somewhere between these extremes. For many sexual populations, nonrandom mating systems (e.g., inbreeding and assortative mating) and geographical subdivisions can greatly increase genetic correlations among individuals and between generations. Correspondingly, many asexual populations are composed of numerous ecologically different clones that arose independently from diversified sexual ancestors. Such diverse clones provide natural experiments that allow biologists to study interactions between fixed genotypes and environments that vary in time and space. In this article, I consider ecological factors that should favor such clonally diverse specialized clones in certain circumstances and a single generalized clone in others. These contrasts help to clarify the benefits of genetic diversity and the processes that generate it. Models for clonal adaptation Asexual organisms flourish in certain environments. Their success has been attributed to a variety of factors, including reproductive efficiency, faithful replication of gen617 T Modes of asexual reproduction in animals o understand the ecology of clones, it is necessary to first consider some genetic, developmental, and demographic consequences of asexual reproduction. Vegetative reproduction (fragmentation, fission, and budding) circumvents egg production and is strictly somatic. Because the products of sexual reproduction, eggs and larvae (seeds in plants), often mediate the ecologically fundamental process of dispersal, whereas vegetative reproduction does not yield such dispersal products, vegetative reproduction is more properly considered a form of growth than of reproduction (Pearse et a1. 1989). Egg production in many invertebrate animals (e.g., cladocerans, brine shrimp, aphids, rotifers, and digenetic trematodes) alternates between sexual and parthenogenetic phases. From an evolutionary perspective, however, such cyclical parthenogenesis is fundamentally sexual. However, some waterfleas (Daphnia) and brine shrimp (Artemia) lose the sexual phase when obligately asexual lineages take over a population (Hebert 1981, Browne and Hoopes 1990). In a strict sense, parthenogenesis (virgin birth) involves only females (Figure la). Cytogeneticists have identified a variety of mechanisms that mediate egg production in parthenogenetic animals (Suomalainen et a1. 1987), but in the context of the adaptive value of clones, it is only relevant that these mechanisms produce either completely homozygous or permanently heterozygous a. Parthenogenesis b. Gynogenesis c. Hybridogenesis clones. Ameiotic (also known as functionally apomictic) parthenogens circumvent or avert chromosomal recombiQ ...--nation (Mendelian segrega~~ tion, assortment, and crossI I ing-over) and transmit an AS" lO intact diploid (or, in many - I ~ cases, polyploid) set of chroQ ..--~~ mosomes to their eggs. FuncI I tionally apomictic parthenogens typically have elevated levels of heterozygosity, particularly in clones that arose Figure 1. All-female modes of reproduction in animals. (a) Parthenogenesis, a strictly as hybrids. By contrast, meiall-female and clonal form of inheritance, is found in reptiles, insects, and many other otic parthenogenesis, which is invertebrate taxa (but not in fish, although they are shown here for convenience). The functionally equivalent to selfgenotypes (AB) of parthenogenetic mothers and daughters are identical. (b) Gynogen- fertilization, leads rapidly to esis, a form of parthenogenesis that requires sperm to initiate cleavage of eggs, occurs complete homozygosity. Some in fish, amphibia, and a wide range of invertebrates. Genetic material from the sperm parthenogenetic Rhabditis is not incorporated or expressed in the offspring. (c) Hybridogenesis, a hemiclonal form nematodes have normal meiof inheritance, occurs in a few fish, frogs, and insects. Only the maternal chromosome otic divisions and restore dipset (A) is transmitted to the eggs; the paternal set (B) is discarded during egg production. loidy by fusing the haploid In each generation, the eggs are truly fertilized by sperm from males of a sexual host. egg nucleus with a polar body As this hypothetical example illustrates, paternal traits (fin spot in B' and tail crescent in B") that segregate in the host population are expressed in the hybrids but are not nucleus. Complete homozygosity occurs in one step in some transmitted through the eggs. parthenogenetic Artemia-the ~ ~~ ~ ~ ~~ ~ ~ ~ era I-purpose genotypes, and generation of specialized genotypes. Although certain hypotheses about clonal adaptation may seem to be contradictory, they are not necessarily so. Geographical parthenogenesis. Asexual organisms are found more frequently at extreme latitudes, at higher, altitudes, at the margins of a species' range, on islands, and in 618 ~~ 0-- if regularly disturbed communities, a pattern commonly known as "geographical parthenogenesis" (Vande! 1928). Parthenogenesis facilitates colonization of new habitats because a single dispersing female can establish a new population. By contrast, at least one male (or stored sperm) and a female are needed to establish a sexually reproducing population. Sexual individuals face additional handicaps finding mates when popu- lation density is low, whereas colonizing parthenogens have" reproductive assurance" (Baker 1965). Consequently, all-female reproduction endows parthenogens with at least twice the net replacement rate of sexual colonists, which devote half of their progeny to males. Conversely, some researchers argue that parthenogens are more abundant in peripheral environments because they are inferior competitors in central BioScience Vol. 48 No.8 Table 1. All-female biotypes of fish in the genus Poeciliopsis. haploid egg nucleus is duplicated and identical meiN umber of otic products are fused . Reproductive mode clones identiAbbreviation Paternal host fied to date Biotype' Regardless of the consequences (heterozygosity or Gynogens (triploid) homozygosity), a preP. 2 monacha-lucida MML P. monacha 3 P. monacha-2 Lucida P. Lucida MLL 3 sumed benefit of partheMLV P. m onacha-Lucida-viriosa P. viriosa nogenesis is faithful repliHybridogens (diploid) cation of the maternal P. monacha-Iucida ML P. lu cida 15 genotype. P. monacha-occidentalis P. occidentalis MO 9 Whatever the mechaP. m onacha-Iatidens MLt P.latidens nism of parthenogenesis, all-female (or unisexual) ' A biotype is a particular combination of genomes from the hybridizing sexual progenitors. For reproduction provides an example, P. 2 monacha-Iucida (or MML) has two chromosome sets from P. monacha and one from P. Lucida. obvious advantage in rapb"?" indicates biotypes that have not been investigated with either a ll ozymic or mitochondria l idly growing populations. DNA markers. A parthenogenetic female has a "twofold advantage" over a corresponding sexual female, who allocates half of her reproductive potential to male offspring. If all else were equal, a parthenogenetic lineage should rapidly replace its sexual counterparts; however, sexual reproduction in fact predominates overwhelmingly in plant and animal taxa (Williams 1975, Maynard Smith 1978). The critical assumption that "all else is equal" (e.g., fecundity, survival, and niche requirements) between sexual and asexual counterparts lies at the heart of this "paradox of sex." However, this assumption may be fundamentally flawed. As I will discuss, animal clones can be ecologically diverse, differing from one another and their sexual counterparts. Many asexual taxa cannot exclude their sexual counterparts because the all-female forms need sperm from sexual males to initiate zygotic development in parthenogenetic eggs. Consequently, sperm-dependent parthenogens are forced to coexist, and possibly compete, with a "sexual host" species. Avariety of spermdependent parthenogenetic modes are found in animals (Beukeboom and Vrijenhoek in press); here I foc us on two forms that occur in fish of the genus Poeciiiopsis (topminnows; family Poeciliidae). Gynogenesis is a strictly clonal form of inheritance-sperm are needed to stimulate development of the zygote but do not contribute to its genotype (Figure 1b). Hybridogenesis is a half-clonal (or hemiclonal) form of inheritancesperm and egg nuclei fuse and paternal genes are expressed in the offspring (Figure 1c), but only the maternal genome is transmitted to the next generation . The genus Poeciliopsis contains six unisexual biotypes that arose as hybrids between Poeciiiopsis monacha and four other sexually reproducing species (Table 1) . The name of each biotype reflects the numbers and kinds of complete chromosome sets contained in the hybrid . The three gynogenetic biotypes transmit an intact triploid genome to their offspring. However, the diploid hybridogenetic biotypes transmit only a haploid, non-recombinant, monacha chromosome set (i.e., a hemiclone) to their eggs. Each hybridogenetic biotype mates with males of a different species and expresses traits from the host species. Genetic surveys of natural populations revealed that these unisexual biotypes contain m ultiple clones (or hemiclones) that arose through independent hybridization events (Vrijenhoek 1979). Much of the evidence I provide for ecological differences among clones and their sexual relatives derives from long-term studies of these remarkable fish (see also Vrijenhoek 1994). areas of a species' range. For example, some asexual lizards appear to be "fugitives" that have escaped from direct competition with their sexual relatives by favoring ecologically marginal habitats (Wright and Lowe 1968). Colonizing parthenogens may gain an additional advantage over colonizing sexuals-namely, protection against inbreeding depression during founder events (Vrijenhoek August 1998 1985). For example, fish of the genus Poeciliopsis were eliminated from an isolated headwater tributary of the RIO Fuerte in Sonora, Mexico, when the stream dried during a severe drought. The tributary was subsequently repopulated by fish that had persisted near springs a few hundred meters downstream. The gynogenetic colonists retained a high level of heterozygosity because of theif clonal reproduction. By con- trast, the sexual colonists had lost all detectable heterozygosity, a probable consequence of a series of founder events during the ·recolonization process. The sexual colonists also exhibited signs of inbreeding depression: an increased parasite load, decreased developmental stability, and a diminished ability to compete with the gynogens. "Heterozygosity assurance" provided the clones with a strong competitive advantage that 619 Figure 1. GeoI • metrical mean fitArithmetic mean, .to =iiL~ =0.50 ,., ness in a tempoGeometrio:: mean _ 0.49 rally fluctuating " 1\ l i 0,8 environment. The i i i ' i i i \ solid and dashed i \ i \ lines represent the 0.6 i j\)\ \ fitnesses of two f \ \ i\ ---------------1 -----+ -..! ' hypotheticalgenotypes living in an 0.4 \\",! \ f \/ environment that iii \ ! ii fluctuates ran0.2 \J V domly over time. Fitnesses of the two genotypes fluctua te around an arithmetic Generations meanofO.5 (dotted line). However, the geometrical mean fitnesses of the genotypes differ. The genotype that fluctuates less (solid line) has a greater geometrical mean fitness (0.49) than the genotype that fluctuates more widely (dashed line, 0.46). The low fitness values have a greater affect on the geometrical mean than the high values. Formulas for the arithmetic (x ) and geometric (x ) means are shown-x represents the fitness value at interval i. g , , d lasted more than 20 generations. until genetic variability was restored to the sexual population (Vrijenhoek 1989b). With the restoration of variability. the sexual population recovered its fitness and regained ecological dominance over the local clones. However, sperm dependence limits the fugitive abilities of gynogens and hybridogens (Beukeboom and Vrijenhoek in press). Es,aping from, or competitively excluding. the sexual host (as almost happened in the previous example) guarantees reproductive failure. Ultimately. a limited supply of sexual males and sperm negates the twofold advantage of allfemale reproduction and prevents gynogens and hybridogens from completely replacing their hosts (Moore and McKay 1971), Consequently, gynogenetic and hybridogenetic fish have relatively limited ranges that are encompassed by the geographical limits of their hosts. By contrast, many parthenogens (e.g .• the cockroach Pycnoscelus surinamensis and the geckonid lizard Lepidodactylus luguhris) have extensive ranges that are completely outside those of their sexual relatives (Parker and Niklasson in press). Gynogens and hybridogens therefore cannot play the role of fugitives. General-purpose genotypes. There have been numerous attempts to define the ecological niche of clonal 620 animals. One model holds that clones perpetuate "general-purpose genotypes" that endow them with a wide niche and broad ecological tolerances; another holds that they possess specialized genotypes with high fitness in a limited range of environments. The General-Purpose Genotype (GPG) model grew from the observation that many broadly distributed asexual weeds can tolerate a wide range of environmental conditions (Baker 1965). It was more explicitly developed to explain the broad geographical range of some parthenogenetic animals (Parker et aL 1977). Lynch (1984) argued that selection in a temporally varying environment should favor general-purpose clones with the highest geometrical mean fitness (Figure 1). Such clones will suffer smaller losses when conditions are poor and should replace specialized clones with limited tolerance of poor conditions. Pboxinus eos-neogaeus, a gynogenetic minnow that arose as a hybrid of Pboxinus eos and Pboxinus neogaeus, may be a general-purpose clone. Schlosser et a1. (1998) compared niche relationships and physical tolerances of a single clone commonly found in northern Minnesota with characteristics of its sexual progenitors. All of the minnows favored the highly oxygenated waters of upland ponds, but the clone was more abundant than the progenitors in collapsed beaver ponds and streams. which have a lower oxygen content . The clone tolerates hypoxic stress better than either of its sexual progenitors, and morphological evidence suggests that it occupies an intermediate trophic niche. Schlosser et aL (1998) hypothesize that the temporal and spatial unpredictability of this environment favored a generalpurpose genotype that occupies a broad intermediate niche and thereby precludes the establishment of additional clones. Only a few additional studies have similarly examined the physiological and ecological breadth of an individual clone, and support for the GPG model is mixed (Parker and Niklasson in press). For example, the wide geographical distribution of many asexual plants is often cited as support for the GPG model (Bierzychudek 1985). However, several criteria should be met before invoking this model. First, the existence of cryptic (i.e., hidden) clones must be ruled out by an examination of appropriate genetic markers. The use of allozymes and DNA fingerprints allowed Schlosser et al. (1998) to verify the existence of a single Pboxinus eosneogaeus done, but many asexual taxa have cryptic clones with substantial differences in ecologically relevant traits. Second, physiological tolerances of individual clones should be tested under environmentally realistic conditions. Performance in the laboratory does not necessarily translate into fitness in nature-witness the mule. a robust animal on the farm that is nevertheless sterile. Finally. the wide geographical distribution of individual clones may not be sufficient evidence for broad physiological or ecological tolerances because such clones might occupy a narrow but universally available niche. For example. some widespread clones of dandelions. earthworms, and cockroaches depend on human transport and habitat disruptionnowadays. a cosmopolitan and abundant niche. Although fluctuating selection in a temporally unpredictable environment should favor broadly tolerant individuals. the present evidence for general-purpose clones of animals is largely inferential. Nevertheless, general-purpose genotypes are believed to arise by at least three BioScience Vol. 48 No.8 means: hybridization and heterosis, polyploidy, and mutations. Hybrid clones and heterosis. The strong associations between asexual reproduction and hybrid origins in the vertebrates and some insects have suggested that cloning fixes hybrid vigor (heterosis), which in turn confers broad ecological tolerance (Schultz 1971, White 1978). Some unisexual organisms have broader tolerance to physical stresses than their sexual counterparts-for example, thermal tolerance is enhanced in Poeciliopsis monacha-lucida (Bulger and Schultz 1979), and P. eos-neogaeus and the frog Rana esculenta have enhanced resistance to hypoxic stress (Tunner and Nopp 1979, Schlosser et al. 1998). But is their enhanced tolerance due to heterosis? To address this question, my colleagues and I synthesized new hybridogenetic strains of Poeciliopsis in the laboratory (Wetherington et al. 1987). On average, the synthesized hybrids were less viable than nonhybrid offspring, and a majority of the hybrids were sterile. All of the fertile hybrids were spontaneously hybridogenetic, however. Although several of the new strains were comparable to the sexual progenitors in several fitness-related traits (e.g., growth rate, early reproductive investment, and survival), none was inherently better, and most were substantially worse. We found no support for the hypotheses that heterosis (or a general-purpose genotype) is a spontaneous product of hybridity. By contrast, a study of laboratory-synthesized hybridogenetic strains of Rana found faster growth rates and greater survival in hybrid larvae, on average, than -in the parental strains (Gutmann et al. 1994). The mean body mass of the hybrid frogs was lower at metamorphosis than that of the parentals, however. Without knowing the combined effects of growth rates, body mass, and survival on lifetime reproduction and survival of these frogs, it may be premature to conclude that hybrid vigor in some traits also confers higher fitness. Again, the example of the mule is instructive. In addition, laboratory studies revealed that some natural hybrid 0genetic strains of P. monacha-lucida grow faster and survive longer than August 1998 their sexual progenitors (Schultz and Fielding 1989), but the differences are not due to heterosis. This conclusion stems from comparisons among laboratory-synthesized P. monachalucida strains.'-Some of the synthetic hybridogens also were fast-growing, but many grew more slowly, and all were equally heterozygous (Wetherington et al. 1987). Differences among the synthetic hybridogens resulted from variance in the combining abilities of the monacha and lucida genomes. The fast-growing natural strains of P. monacha-lucida represent "good combinations" that have survived. Biologists must therefore exercise caution in making inferences about heterosis and fitness from comparative studies of natural clones and their sexual relatives. We see only nature's successful clonesnot the failures that natural selection quickly purges. Instead of heterosis, the association between unisexuality and hybridization in the vertebrates may result from hybrid dysgenesis, in which hybridization between divergent species and populations leads to disrupted meiosis and sterility (Vrijenhoek 1989a). Clearly, hybrid sterility results in selection for spontaneous "cytogenetic accidents" that rescue egg production and restore or retain diploidy. These accidents can quickly become established ifcoupled with all-female reproduction and a concomitant twofold reproductive advantage. Polyploidy and general-purpose clones. The majority of unisexual vertebrates and insects are polyploids (Suomalainen et al. 1987), and elevated ploidy has been linked to general-purpose genotypes. Triploid clones of the waterflea Daphnia pulex are more cold tolerant and occur at higher latitudes than diploid clones (Beaton and Hebert 1988). One possible explanation for polyploid superiority is that selection among clones has fixed genomic combinations that express the best characteristic of each species in the hybrid. Nevertheless, the association between asexuality and elevated ploidy provides no better evidence for an inherent superiority of polyploids than the association with hybridization provides for hybrid superiority. Indeed, the polyploid association may also result from dysgenesis. Most diploid organisms occasionally produce unreduced eggs, which, if fertilized, result in triploid progeny that are typically sterile. Such events create another window of opportunity for the selection of "cytogenetic accidents" that can restore egg production. Another explanation for the asso~ ciation between asexuality and polyploidy is that prior establishment of parthenogenesis facilitates the elevation of ploidy because meiosis has already been circumvented. Indeed, triploid forms of Poeciliopsis arose by adding a third genome to a diploid unisexual ancestor (Schultz 1969). For example, P. monachalucida-viriosa (3n = 72) added a viriosa genome (In ~ 24) to a diploid P. monacha-Iucida ancestor (2n = 48). Still, for most asexual polyploids we do not know whether asexuality or polyploidy came first. The enhanced performance of some natural polyploids over their diploid counterparts may also be a product of selection among clones and fixation of the best genomic combinations from sexual ancestors, rather than of elevated ploidy itself. Mutations and clonal evolution. In theory, general-purpose genotypes could arise within an asexual lineage if mutation rates are sufficient (Lynch and Gabriel 1983). The discovery of ancient asexual taxa with numerous divergent species would provide evidence for the potency of mutational advance, but few taxa meet this requirement. The best known exception is the rotifer class Bdelloidea, which contains more than 350 asexual species in 18 genera. Bdelloid clones include enormous numbers of individuals and may have pandemic distributions. They probably avoid extinction because they can form a dormant stage when conditions are poor and because they have excep~ tional dispersal abilities. Larger organisms, with more limited population sizes, are more likely to suffer "mutational meltdown" (also known as Muller's Ratchet). Meltdown occurs in asexual populations because mildly deleterious mutations will tend to accumulate and lead to a progressive deterioration of fitness as clones with low mutational loads are lost by chance (Lynch et al. 1993). Apart from the bdelloids, little 621 nists reaching an underexploited environment increase niche breadth through behavioral plasticity (i.e., the within-phenotype component). As population density and competition for resources increase, ecological breadth can expand again by selection for genes that enhance plasticity, and by diversifying selection on genetic variation that controls Resources After selection the between-phenotype component of niche breadth. Diversification is Sexual population ~ Clone I Clone V ~ slowed in sexual populations, however, because novel genotypes that can effectively exploit marginal re--- "': sources are reshuffled in each gen] : ~:l eration, and the majority of sexual 5 i~ __ _______________ L~: __ offspring regress phenotypically to the population's mean. Roughgarden Resource distribution suggested that cloning would be a rapid way to freeze divergent genotypes responsible for the betweenFigure 2. The Frozen Niche·Variation model of clonal establishment. Although phenotype component of niche originally developed to explain clones that arose from hybridization, the model also breadth and to resolve the conflict applies to clones of nonhybtid origin (Weeks 1993). Resources are assumed to be between diversifying selection and uniformly distributed (dashed line), and the utilization functions of a sexual recombination. population and several clones are assumed to be normally distributed (solid lines) According to the FNV model, rebut different in width. New clones (I through V) are frozen from the phenotypic distribution of the sexual ancestors. Natural selection will fix clones that exploit current origins of clones can freeze marginal resources and overlap minimally with the sexual progenitors. Simulation the between-phenotype component studies revealed that clonal invasion of the sexual niche begins at its margins and of variation that exists in genetically slowly progresses towards the center. variable sexual progenitors (Figure 2). Interclonal selection subsequently acts on this array of genotypes, fasubstantive evidence exists for truly enon in finite populations (Lynch et voring clones fhat have minimal niche ancient and diversified asexual taxa a1. 1993) may explain the virtual overlap with established clones and (Judson and Normark 1996). A absence of truly ancient clones of with the sexual progenitors. On a local scale, this process will generate hybridogenetic Poeciliopsis lineage vertebrates and arthropods. an assemblage of clones that can has persisted for at least 100,000 years, but this is young compared to Frozen variation. Most of the geno- successfully coexist with one another the ages of related sexual species, typic diversity seen in asexual verte- and with the sexual progenitors. If which have persisted for millions of brate, arthropod, and snail popula- individual clones have narrower years (Quattro et al. 1992). Diver- tions arises from multiple origins of niches than the sexual population, gence of mitochondrial DNA se- clones from sexual ancestors, rather then two predictions follow: first, a q uences suggests that some asexual than from mutational accumulation single clone should have limited comsalamanders and clams may be sev- within asexual lineages (Crease et al. petitive impact on genetically varieral million years old, but the nuclear 1989, Avise et al. 1992, Dybdahl able sexual relatives (i.e., competigenomes associated with these "mito- and Lively 1995). Discoveries of such tion is asymmetrical); second, a chondrial clones" may not be ancient. diversity in unisexual Poeciliopsis diverse array of specialized clones Instead, their nuclear genomes ap- led me to propose the Frozen Niche- could eclipse the sexual niche and pear to be refreshed periodically by Variation (FNV) model (Vrijenhoek competitively displace the progenitors. the incorporation of new chromo- 1979,1984). This model grew from Comparisons of monoclonal (single some sets from the sexual gene pool. ideas expressed by Roughgarden clone) versus multic10nal (many Elevated ploidy may buffer against (1972) on the evolution of niche clones) populations of Poeciliopsis the meltdown of asexual lineages breadth. He hypothesized that "eco- support these predictions (Vrijenbeca use adding a new genome from logical release" (i.e., an increase in hoek 1979). Ghiselin (1974) had previously the sexual gene pool can mask accu- niche breadth commonly found in mulated genetic lesions (Suomalainen colonizing species faced with reduced suggested that a genetically diverse et a1. 1987). Overall, however, clones interspecific competition) results sexual population should be more with many genes and small popula- from changes in the within- and be- efficient than a single clone at extion sizes are more likely to decay tween-phenotype components of tracting resources from a heterogethan advance from mutations. The morphological and behavioral varia- neous environment (also known as the rapidity of the meltdown phenom- tion. He suggested that the first colo- "Tangled Bank" model; Bell 1982). Before selection ~ ~=C 622 I r------------------------------~------~ ~~ ! BioScience Vol. 48 No.8 Consequently, sexual competitors should be able to coexist with a clonal assemblage, so long as the sexual niche remains wider than the combined asexual niche (Case and Taper 1986). Evidence for asymmetrical competition between sexual and asexual forms is found in lizards, frogs, and fish (Vrijenhoek 1979, Case 1990, Semlitsch 1993). Perhaps the most compelling evidence for the competitive superiority of sexual diversity is found in geckonid lizards on South Pacific islands (Petren et aJ. 1993). A single gecko clone dominated most islands until it was competitively displaced by recent sexual invaders. A frozen niche may be vulnerable in the face of novel sexual invaders. Another feature of the FNV model is that clones lost through competition, mutational meltdown, or stochastic events can be replaced if new asexual genotypes are periodically frozen from sexual progenitors. If new asexual lineages arise frequently, a diverse assemblage of clones could eclipse the sexual niche and cause extinction of the progenitors. However, most animal taxa appear to be resistant to the production of clones-perhaps because sexual lineages that were prone to generating clones were rapidly driven to extinction by the clones they produced (Nunney 1989). Computer simulations of the FNV model (Weeks 1993) revealed that if clones do not arise too frequently, and if natural resources are distributed uniformly, then clones that exploit marginal resources will be favored over clones that compete more directly with the sexual population (Figure 2). Clones with "marginal" phenotypes compete with smaller numbers of sexual individuals that are generated in the tails of the phenotypic distribution. Clones with "central" phenotypes may be capable of outcompeting sexual individuals at the center of the resource distribution, but "centralized" sexual phenotypes are regenerated in each generation by recombination. These simulations produced results that are consistent with the overall pattern of geographical parthenogenesis-clones are more frequent in marginal environments. A similar pattern exists on a microhabitat scale with unisexual August 1998 Poeciliopsis (Vrijenhoek 1984). In populations composed of a single clone, the unisexual inividuals are most abundant in peripheral pools, and they are nearly absent in mainstream areas~ with some current, where the sexual" individuals dwell. In multiclonal populations, the unisexual fish completely dominate pools and mainstream areas. In cion ally diverse populations, unisexual females greatly outnumber the sexual females and would probably replace them altogether if sperm did not become limiting for these hybridogenetic fish. The main assumption of the FNV model is that clones can freeze variation that exists in the gene pool of the sexual progenitors. We tested this assumption by examining laboratory-synthesized hybridogenetic strains of Poeciliopsis. The differences in morphology, physiology, life-history traits, and behavior observed among these strains clearly demonstrate the potential for freezing ecologically relevant phenotypic variation (Schultz and Fielding 1989, Wetherington et al. 1989b, Lima and Vrijenhoek 1996, Lima et aJ. 1996). Identifying similar differences among natural clones of Poeciliopsis has been a focus of our research efforts during the past 25 years (reviewed by Schultz and Fielding 1989, Vrijenhoek 1990). Recent studies of lizards, frogs, snails, brine shrimp, and cladocera provide further evidence for ecological diversification among naturally occurring clones (Browne and Hoopes 1990, Case 1990, Weider 1993, Jokela et a!. 1997, Semlitsch et al. 1997). I focus the remaining discussion on recent studies of unisexual fish. In particular, I examine hypotheses that unisexual organisms of hybrid origin tend to occupy an intermediate niche and that individual clones are phenotypically inflexible. Hybrid clones and an intermediate niche. Moore (1977) expressed an alternative view of clonal adaptation, hypothesizing that unisexuals of hybrid origin can escape direct competition with their sexual progenitors by occupying an intermediate niche. The gynogenetic minnow clone (Phoxinus eos-neogaeus) found in northern Minnesota is believed to occupy such an intermediate niche because its feeding structures are generally intermediate (in a multivariate sense) to those of its progenitors, P. eos and P. neogaeus (Schlosser et al. 1998).ltis a mistake, however, to assume that fish hybrids invariably express intermediate phenotypes (Ross and Cavender 1981). As Haldane (1932) noted, hybridization "may merely lead to new combinations of the characters of the species or groups which hybridize, but ... it may also produce something entirely fresh." For example, the laboratorysynthesized hybridogenetic strains of Poeciliopsis monacha-Iucida were broadly intermediate to the progenitors for most quantitative traits, but several strains possessed phenotypes that deviated greatly from the intermediate mean (Wetherington et al. 1989b, Lima and Vrijenhoek 1996, Lima et al. 1996). In these cases, behaviors and pigmentation patterns were as extreme as the parental forms (i.e., the hybrids expressed dominant phenotypes). If an uncontested intermediate niche exists between hybridizing sexual progenitors, selection will probably fix a clone with the appropriate intermediate traits. In this sense, Moore's (1977) hypothesis of an intermediate niche for unisexual hybrids represents a special case of frozen niche-variation. However, ecological intermediacy is not an inevitable consequence of hybridization, as I shall discuss later. It may also be a mistake to assume that niche position is correlated with morphology. For many species, behavioral plasticity plays a greater role than morphology in determining the use of food and spatial resources. For example, natural hemiclones of Poeciliopsis monacha-lucida are broadly intermediate to P. monacha and P. lucida for the number of inner teeth on the dentary bone (Figure 3). These tiny teeth also occur on the premaxillary and pharyngeal bones, where they produce an abrasive surface that helps the fish to manipulate and swallow insect larvae. Although two P. monacha~Jucida hemiclones, designated MLiVII and MLlVIII, both have intermediate numbers of these teeth, they differ greatly in predatory efficiency. Hemiclone MLIVII is intermediate in its prey-handling ability, and its natural diet is also broadly intermediate (Weeks et al. 623 Figure 3. Dentition and preda- a tion efficiency in sexual and hybridogenetic biotypes of Poeciliopsistoprninnows from the Arroyo de Jaguari (Rio Fuerte, Sonora, P.lucida Mexico). (a) The P. monacha left dentary bone is illustrated for each biotype P. monacha-Iucida {modified after b 4.5 Vrijenhoek and Schultz 1974}. (b) Relationships between the mean u number of inner ! 4.0 P.lucida teeth on the left •E dentary bone and MLNII handling time (the mean time MLNIII between attacking and swallowP. monacha ing chi rona mid larvae; original 3.0 +--r--'--~-'----'-~-~~r--'--, data from Weeks 20 40 60 80 100 et al. 1993). ErNumber of teeth ror bars represent one standard error on either side of the mean. The P. monacha-lucida biotype includes two hemiclones, MLiVII and MLlVIII. + + ~ + 1992). If MLlVlI were the only unisexual fish found in its native stream, it might be considered evidence for the hypothesis of an intermediate unisexual niche. However, it coexists with hemiclone MLIVIII, which is a more efficient predator than either of its sexual progenitors. Thus, the intermediate trophic morphology of MLIVIII does not constrain this fish to an intermediate diet. As the abundance of various kinds of food changes seasonally, these fish correspondingly shift their diets; however, the degree of dietary plasticity differs greatly among the members of this fish assemblage. One sexual species, P. lucida, is relatively rigid in its feeding behavior-it is a bottom-feeding detritivore. The other sexual species, P. monacha, is more flexible-it is the most herbivorous member of this assemblage during the dry season and the most predaceous following the rainy season, when insect larvae are abundant. Hemiclones MLlVlI and MLlVIII both obtain intermediate quantities of insects when larvae are abundant, 624 + but when larvae are scarce, MLIVII increases its herbivory and MLIVIII becomes more predaceous. In the laboratory, MLIVIII is an aggressive predator that interferes with the foraging of other fish in this assemblage, often stealing insect larvae from fish that are less efficient at handling prey. Consequently, as Haldane suggested, hybridization appears to have resulted in something that is "entirely fresh" and not seen in either of the parental species. Phenotypic plasticity. Baker (1965) suggested that plasticity in some characters may be required to stabilize fitness in a variable environment. Developmental plasticity appears to be a common characteristic of widely distributed weeds and, presumably, of general-purpose genotypes. For example, some Daphnia species develop protective spines when raised in the presence of predators. In contrast, phenotypically rigid genotypes are expected to show greater variance in fitness across fluctuating environments and should, therefore, be subject to a higher rate of extinction. Consequently, natural selection should favor mutations that increase the adaptive plasticity of clones and lead to the evolution of general-purpose genotypes (Lynch 1984). Alternatively, cloning could freeze the capacity for phenotypic plasticity from variation in the sexual progenitors, as demonstrated by the laboratory-synthesized hybridogens of Poeciiiopsis (Wetherington et al. 1989a). All of the synthetic strains grew more slowly when reared on a low-protein diet. This finding alone is not surprising, but one strain suffered substantially less than the others.1t was the slowest-growing clone when raised on a high-protein diet and the fastest-growing clone when raised on a low-protein diet. Such a clone might suffer the least during poor conditions and consequently have the highest geometric mean fitness in a fluctuating environment. However, these synthetic hemiclones do not exist in nature. It seems likely that natural clones froze similar life history differences from variation in the sexual ancestors (for examples, see Schultz and Fielding 1989). The capacity for phenotypic plasticity could be frozen because clones are genotypes. involving thousands of interacting genes that affect complex mixtures of traits. The rigid dentition and plastic feeding behavior of hemiclone MLIVIII illustrate this complexity. Studies of the laboratorysynthesized hybridogens revealed that complex feeding behaviors encompassing the range expressed by natural hemiclones MLIVII and MLI VIII could be frozen from the gene pools of the sexual progenitors (Lima 1998). As biologists continue to study clonal organisms from a multivariate ecological perspective, some clones will likely turn out to be food generalists and habitat specialists, some will be food specialists and habitat generalists, and some will be specialists or generalists for both food and habitat. Plasticity may be favored in traits that interact with seasonally varying resources , and rigidity may be favored in traits that reduce interspecific competition. The gene pools of sexual species such as P. monacha store the historical solutions to all of these contingencies. The clonal forms that this species BioScience Vol. 48 No.8 has spawned freeze this in1.0 formation and use it to great .----------. ... MMUI effect during the short term, because they numerically O.B dominate the fish communi\ ties in rivers in which recur~ .~ 0-. . . \ rent origins of new clones 0.6 ,-----'-- ............ \ w are possible (Vrijenhoek 0 ~ P. monacha 1979). Clonal diversity that \ is periodically frozen from ~~ 0.' \ the sexual gene pool may be a: \ similarly responsible for the MMUII 0.2 ecological success of many asexual taxa. If this hypothesis is true, it may be hard to 0.0 ~--------,--------,--escape the conclusion that a Heat Cold Hypoxia little sex (i.e., the generation Type of stress of novel recombinant genotypes) is also good for asexual taxa (see also Green and Figure 4. Relative rates of survival under three kinds of environmental stress in a sexual species and two hybridogenetic Noakes 1995). stress only, we might have concluded that clone MMLI 11 is a broadly tolerant, general-purpose genotype. Its wide distribution in several headwater tributaries of the Rios Fuerte and Sinaloa is consistent with this interpretation. If, on the other hand, we had studied hypoxic stress only, we might have concluded that MMLlII is narrowly adapted. Clone MMLIII also has narrow feeding behavior-it is a "drift feeder" that prefers to feed on suspended prey items found in shallow areas with some current (Schenck and Vrijenhoek 1989). Clearly, MMLIII is a complex mixbiotypes of Poeciliopsis. The relative surviVal value equals the ture of generalist and speFitness variation in time and mean survival rate of each type of fish divided by the maximum cialist traits. In many resurvival rate (from Vrijenhoek and Pfeiler 1997). space. Several recent studies spects, the corresponding of unisexual lizards, brine clone, MMLII, appears to be shrimp, snails, fish, frogs, and water- tolerance, feeding behavior, habitat more specialized-it has narrow therfleas have attempted to test predic- preference, and other characteristics. mal tolerances and a restricted range tions of the GPG and FNV models as Researchers may reach erroneous in the Rio Fuerte. However, it is the if they were mutually exclusive alter- conclusions about clones if they ex- most tolerant of these fishes to hynatives (Browne and Hoopes 1990, amine only a few traits. A recent poxic stress, and its feeding and Weider 1993, Bolger and Case 1994, study of two gynogenetic clones swimming behaviors are least afJokela et a1. 1997, Semlitsch et a1. (MMLII and MMLlII of Poeciliopsis fected by the presence or absence of 1997, Schlosser et al. 1998). How- 2 monacha-lucida) that coexist in water currents (Schenck and Vrijenever, the two models do not neces- springs and streams of southern hoek 1989, Vrijenhoek and pfeiler sarily lead to alternative predictions, Sonora, Mexico, illustrates this point. 1997). The behavioral and physibecause they are based on different Flash floods scour Sonoran streams ological complexity of these fishes assumptions about environmental during the rainy season, and large suggests that claims about "generalheterogeneity in time and space. portions of the streambeds are with- ist" or "specialist" clones that are Simple contrasts of these models as- out water during the long dry season based on studies of only a few traits sume that fitness variation in time in this arid region. Consequently, should be made cautiously. Perhaps the most significant lesshould favor general-purpose geno- some fish must survive in stagnant types, whereas heterogeneity in food residual pools in which water tem- son to emerge from our studies is and in spatial resources should favor peratures exceed 40°C and dissolved that the sexual species, P. monacha, multiple specialized clones. As dis- oxygen concentrations drop to le- may be the most generalized of the cussed above. most studies of thal levels. Other fish survive in three fishes. It has the broadest diet multiclonal populations of unisexual springs and seeps, or in shady pools (Schenck and Vrijenhoek 1989) and lizards, brine shrimp, snails, frogs, and crevices. During cold winter the best ability to tolerate shifts in and waterfleas have supported the mornings, most fish are torpid, environmental stresses. Although P. FNV model, and a study of mono- whereas others swim actively near monacha is not the best at surviving clonal populations of Phoxinus eos- the effluents of natural hot springs. heat, cold, or hypoxic stress (Figure neogaeus was consistent with the We tested the tolerance of the two 4), it is generally not the worst. Its GPG model. Considering the evi- clones and their sexual host, P. tendency to be intermediate is a condence given below, however, even monacha, to heat, cold, and hypoxic sequence of averaging the survival the Phoxinus example may not be stress (Vrijenhoek and Pfeiler 1997). differences across many genotypiNo single type of fish outperformed cally unique individuals (Vrijenhoek inconsistent with the FNV model. Predictions based on the GPG and the others across all three stresses (Fig- etal.1992). Consequently, the sexual FNV models are confounded in natu- ure 4 )--clone MMLlII had the highest species may have the highest georal environments that vary in both survival rate during heat and cold metrical mean fitness in these seatime and space. As I have argued, stress, MMLII was best at surviving sonally and spatially heterogeneous natural clones are complex mixtures hypoxic stress, and P. monacha gen- desert streams. The two clones, on the other hand, are fixed genotypes of specialized and generalized traits erally was average. If we had studied heat and cold that exhibit much greater variance in affecting life history, physiological " Y '\--0 • August 1998 625 survival across these stresses. Although the clones have highly elevated levels of heterozygosity (as a consequence of their hybrid origins), they do not appear to have broadly enhanced physiological tolerances. The wide fluctuations in survival of the two clones result in lower geometrical mean fitnesses. Clonal limits and the benefits of sex Genotypic and phenotypic differences among individuals are the essence of sexual reproduction and may be required for species locked into coevolutionary struggles with rapidly evolving biological enemies. The Red Queen in Lewis Carroll's Through the Looking Glass advised Alice that "it takes all the running you can do, to keep in the same place." Genetic diversity is essential for keeping up with parasites and pathogens that evolve rapidly to exploit the most common host phenotypes. Rare host phenotypes may escape infection and thereby gain a temporary advantage until they too are abundant and become the focus of coevolving parasites. This cycle of frequency-dependent fitness preserves genetic diversity in the host population and favors the maintenance of sex (Hamilton et al. 1981). Consequently, highly abundant clones in a mixed reproductive complex should be more heavily parasitized than the unique individuals that make up a sexual lineage. Support for the Red Queen model has been found in several studies of cion ally reproducing animals, including Poeciliopsis (Lively et al. 1990). Many biologists believe that the Red Queen model provides one of the most powerful ecological explanations for the maintenance of sex and genetic diversity in higher organisms (Ridley 1993). Ultimately, clones are fixed genotypes with limited abilities to respond to ca pricious biotic and physical environments. Natural selection acts on the aggregate of gene interactions in clones, rather than the average effects of independent genes, as in sexual species. Naturally occurring clones are successful genotypes that involve the collaboration of thousands of genes. Interactions be626 tween these clones and a variable environment may be rigid for some traits (e.g., morphology) and plastic for others (e.g., behavior). Certain clones are generalists along some niche dimensions and specialists along others. Although the gynogenetic fish clone MMLIII comes closest, we have found no truly multidimensional, general-purpose genotype among clones of Poeciliopsis. The divergent clonal lineages studied to date represent only a small fraction of the genotypic combinations that have resulted from hybridization and polyploidization events in this fish. Natural selection rapidly purges the bad genotypic combinations and preserves clones with compatible combinations. The clonal diversity that is seen in natural Poeciliopsis populations urtdoubtedly represents a biased subset of genotypes that have passed this first test of natural selection. However, even the good combinations must be lucky enough to find an uncontested niche. Clonal invasion of a sexual population appears to begin at the weakly contested margins of its ecological niche (Weeks 1993). Some unisexual taxa that arose as interspecific hybrids may occupy a weakly contested intermediate niche between their sexual progenitors; however, hybrids are not necessarily intermediate for all characteristics, as exemplified by the predatory efficiency of hemiclone MLIVIII and the thermal tolerance of clone MMLlII. The GPG model predicts that environmental fluctuations will favor the most broadly tolerant genotype (Lynch 1984); nevertheless, asexual populations often contain multiple clones. How can this apparent contradiction be resolved? Perhaps genetic models provide an inadequate view of clones. It may be more appropriate to view clones as we view species in a biological community, rather than as genes in a gene pool. Community ecologists argue that intermediate levels of environmental disturbance can facilitate the maintenance of species diversity (Connell 1978), and modeling studies reveal that intermediate levels of disturbance can facilitate the maintenance of clonal diversity if clones differ in competitive abilities and reproduc- tive rates (Sebens and Thorne 1985). A promising experimental study with Daphnia clones supports these basic predictions (Weider 1993). Intermediate levels of disturbance maintained the greatest diversity of Daphnia clones, whereas high and low levels of disturbance resulted in less diversity. Long-term studies of these clones are needed to identify the specific tradeoffs between the reproductive rates and competitive abilities of clones. Nevertheless, a pioneering study of dandelions (Taraxacum officina/e) provides a model for clonal coexistence under intermediate disturbance (Sol brig 1971). One dandelion clone (A) matures early and produces more seeds, whereas the other clone (D) is a superior competitor at high densities. Without disturbance, clone D always outcompetes clone A. With constant disturbance, such as mowing or grazing, competitive abilities are unimportant, and clone A can win. Sol brig (1971) hypothesized that the clones can coexist because intermediate levels of disturbance favor each clone at different times and in different places. It would be relatively easy to maintain such clones with dispersal among patches in a temporally and spatially heterogeneous environment. Over the long term, however, it may not be important for a particular genotype to be the best competitor or to have the greatest reproductive output in a particular environment, so long as it is not often the worst genotype in alternative environments. Unlike cloning, sex is not an efficient way to consistently produce the most fit genotype in a predictable environment, but it avoids consistently producing the worst genotype when conditions inevitably change (Vrijenhoek and Pfeiler 1997). The average, yet flexible, abilities of P. monacha (the matriarchal ancestor of all Poeciliopsis clones) to survive opposing environmental stresses may provide this species with the highest geometrical mean fitness in its temporally and spatially varying habitats. Sexual species of Poeciliopsis persist for many millions of years, and their evolutionary longevity may be a consequence of phenotypic regression that slows the adaptive response to fluctuating selection pressures and thereby avoids a higher BioScience Vol. 48 No.8 probability of extinction suffered by fixed genotypes (Eshel and Feldman 1970). Genetic variability in P. monacha also plays a critical role in its ability to live with parasites (Lively et al. 1990), which probably contribute more than the physical environment to fluctuations in fitness and the direction of selection. Clonal organisms are natural evolutionary experiments. One of the most valuable lessons learned from these experiments is that clones can freeze and faithfully replicate genotypic differences that exist in sexual populations. Studies of natural and laboratory-synthesized clones expose the extraordinary variability that exists in gene pools of sexual species. The persistence of sexual progenitors faced with competition from allfemale clones supports the hypothesis that genotypic diversity provides ecological benefits that can compensate for the costs of sex (Williams 1975). Meiosis and outcrossing may also provide direct genetic benefits, such as enhanced repair of mutations and "'rejuvenation" of the genome (Michod 1995). Evidence for the immediate genetic benefits of sex may be difficult to obtain in studies of natural populations. but the possibility of such benefits warrants serious experimental investigation before we embark on the wholesale cloning of mammals. Acknowledgments I thank my former students and colleagues who helped sample fish in Mexico and rear strains so diligently in the laboratory. Mostly, I thank R. J. Schultz, who pioneered studies of unisexual Poeciliopsis and stimulated many of the studies summarized herein. The research was funded (1974-1992) by grants from the National Science Foundation and the New Jersey Agricultural Experiment Station. References cited AviseJC, QuattroJM, Vrijenhoek RC. 1992. Molecular clones within organismal dones. Evolutionary Biology 26: 225246. Baker HG. 1965. Characteristics and modes of origin of weeds. Pages 147-172 in Baker HG, Stebbins GL, eds. Genetics of Colonizing Species. New York: Academic Press. Beaton MJ, Hebert PDN. 1988. Geographic August 1998 parthenogenesis and polyploidy in Daphnia pulex. American Naturalist 132: 837845. Bell G. 1982. The Masterpiece of Nature: The Evolution and Genetics of Sexuality. Berkeley (CA): University of California Press. Beukeboom L, Vrijenhoek RC. In press. Evolutionary genetics and ecology of spermdependent parthenogenesis. Journal of Evolutionary Biology. Bierzychudek P. 1985. Patterns in plant parthenogenesis. Experientia 41: 1255-1264. Bolger DT, Case TJ. 1994. Divergent ecology of sympatric clones of the asexual gecko, Lepidodactylus lugubris. Oecologia 100: 397-405. Browne RA, Hoopes CWo 1990. Genotypic diversity and selection in asexual brine shrimp (Artemia). Evolution 44: 10351051. Bulger AJ, Schultz RJ. 1979. Heterosis and interclonal variation in thermal tolerance in unisexual fish. Evolution 33: 848-859. Case T. 1990. Patterns of coexistence in sexual and asexual species of Cnemidophorus lizards. Oecologia 83: 220-227. Case TJ, Taper ML. 1986. On the coexistence and coevolution of asexual and sexual competitors. Evolution 40: 366-387. Connell JH. 1978. Diversity in tropical rain forests and coral reefs. Science 199: 13021310. Crease TJ, Stanton OJ, Hebert PDN. 1989. Polyphyletic origins of asexuality in Daphnia pulex. II. Mitochondrial-DNA variation. Evolution 43: 1016-1026. Dybdahl MF, Lively CM. 1995. Diverse endemic and polyphyletic clones in mixed populations of the freshwater snail, Potamopyrgus antipodarum. Journal of Evolutionary Biology 8: 385-398. Eshel I, Feldman MW. 1970. On the evolutionary effect of recombination. Theoretical Population Biology 1: 88-110. Ghiselin MT. 1974. The Economy of Nature and the Evolution of Sex. Berkeley (CA): University of California Press. Green RF, Noakes DLG. 1995. Is a little bit of sex as good as a lot? Journal of Theoretical Biology 174: 87-96. Gutmann E, Hotz H, Semlitsch RD, Guex G-D, Beerli P, Berger L, Uzzell T. 1994. Spontaneous heterosis in larval life-history traits of hemiclonal water frog hybrids. Zoologica Poloniae 39: 527-528. HaldaneJBS. 1932. The Causes of Evolution. New York: Longman. Hamilton WD, Henderson P, Moran N. 1981. Fluctuation of environmental and coevolved antagonist polymorphism as factors in the maintenance of sex. Pages 363381 in Alexander RD, Tinkle D, eds. Natural Selection and Social Behavior. New York: Chiron Press. Hebert PDN. 1981. Obligate asexuality in Daphnia. American Naturalist 117: 784789. Jokela J, Lively CM, Fox JA, Dybdahl MF. 1997. Flat reaction norms and 'frozen' phenotypic variation in clonal snails (Potamopyrgus antipodarum). Evolution 51: 1120-1129. Judson OP, Normark BB. 1996. Ancient asexual scandals. Trends in Ecology & Evolution 11: 41-46. Lima NRW. 1998. Genetic analysis of predatory efficiency in natural and laboratory made hybrids of Poeciliopsis (Pisces: Poeciliidae). Behaviour 135: 83-98. l.ima NRW, Vrijenhoek RC. 1996. Avoidance of filial cannibalism by sexual and clonal forms of Poeciliopsis (Pisces: Poeciliidae). Animal Behavior 51: 29330t. Lima NRW, Koback CJ, Vrijenhoek RC. 1996. Evolution of sexual mimicry in sperm-dependent clonal forms of Poeciliopsis (Pisces: Poeciliidae). Journal of Evolutionary Biology 9: 185-203. Lively CM, Craddock C, Vrijenhoek RC. 1990. The Red Queen hypothesis supported by parasitism in sexual and clonal fish. Nature 344: 864-866. Lynch M. 1984. Destabilizing hybridization, general-purpose genotypes and geographical parthenogenesis. Quarterly Review of Biology 59: 257-290. Lynch M, Gabriel W. 1983. Phenotypic evolution and parthenogenesis. American Naturalist 122: 745-764. Lynch M, Burger R, Butcher D, Gabriel W. 1993. The mutational meltdown in asexual populations. Journal of Heredity. 84: 339344. Maynard Smith J. 1978. The Evolution of Sex. Cambridge (UK): Cambridge University Press. Michod RE. 1995. Eros and Evolution: A Natural Philosophy of Sex. Reading (MA): Addison Wesley. Moore WS. 1977. An evaluation of narrow hybrid zones in vertebrates. Quarterly Review of Biology 52: 263-277. Moore WS, McKay FE. 1971. Coexistence in unisexual-bisexual species complexes of Poeci/iopsis (Pisces: Poeciliidae). Ecology 52: 791-799. Nunney L 1989. The maintenance of sex by group selection. Evolution 43: 245-257. Parker ED Jr., Niklasson M. In press. Genetic structure and evolution in parthenogenetic animals. In Singh R, Krimbas C, eds. Evolutionary Genetics from Molecules to Morphology. Cambridge (UK): Cambridge University Press. Parker ED Jr., Selander RK, Hudson RO, Lester LJ. 1977. Genetic diversity in colonizing parthenogenetic cockroaches. Evolution 31: 836-842. Pearse JS, Pearse VB, Newberry AT. 1989. Telling sex from growth: Dissolving Maynard Smith's paradox. Bulletin of Marine Science 45: 433-446. Petren K, Bolger DT, Case TJ. 1993. Mechanisms in the competitive success of an invading sexual gecko over an asexual native. Science 259: 354-358. Quanro JM, AviseJC, Vrijenhoek RC. 1992. An ancient clonal lineage in the fish genus Poeciliopsis (Atherini{ormes: Poeciliidae). Proceedings of the National Academy of Sciences of the United States of America 89: 348-352. Ridley M. 1993. The Red Queen: Sex and the Evolution of Human Nature. New York: Penguin Books. Ross MR, Cavender TM. 1981. Morphological analysis of four experimental intergeneric cyprinid hybrid crosses. Copeia 1981: 377-387. Roughgarden J. 1972. Evolution of niche 627 width. American Naturalist 106: 683-718. Schenck RA, Vrijenhoek RC. 1989. Coexistence among sexual and asexual forms of Poecifiopsis: Foraging behavior and microhabitat selection. Pages 39-48 in Dawley R, Bogart J, cds. Evolution and Ecology of Unisexual Vertebrates. Albany (NY): New York State Museum. Bulletin no. 466. Schlosser IJ, Doeringsfeld MR, Elder J, Arzayus LF. 1998. Niche relationships of clonal and sexual fish in a heterogeneous landscape. Ecology 79: 953-968. Schultz RJ. 1969. Hybridization, unisexuality and polyploidy in the teleost Poeciliopsis (Poeciliidae) and other vertebrates. American Naturalist 103: 605-619. ___ . 1971. Special adaptive problems associated with unisexual fishes. American Zoologist 11: 351-360. Schultz RJ, Ficlding E. 1989. Fixed genotypes in variable environments. Pages 32-38 in Dawley R, Bogart J, eds. Evolution and Ecology of Unisexual Vertebrates. Albany (NY): New York State Museum. Bulletin no. 466. Sebens KP, Thorne BL 1985. Coexistence of clones, clonal diversity, and the effects of disturbance. Pages 357-398 in Jackson JBC, Buss LW, Cook RE, eds. Population Biology and Evolution of Clonal Organisms. New Haven (ef): Yale University Press. Semlitsch RD. 1993. Asymmetric competition in mixed populations of tadpoles of the hybridogenetic Rana esculenta com- plex. Evolution 47: 510-519. Semlitsch RD, Hotz H, Guex G-D. 1997. Competition among tadpoles of coexisting hemiclones of hybridogenetic Rana esculenta: Support for the Frozen Niche Variation model. Evolution 51: 12491261. Sol brig O. 1971. The population biology of dandelions. American Scientist 59: 686694. Stanley SM. 1975. Clades versus clones in evolution: Why we have sex. Science 190: 382-383. Suomalainen E, Saura A, Lokki J. 1987. Cytology and Evolution in Parthenogenesis. Boca Raton (FL): CRC Press. Tunner HG, Nopp H. 1979. Heterosis in the common European water frog. Naturwissenschaften 66: 268-269. Vandd A. 1928. La parthenogenese geographique contribution a ]'etude biologique et cytologique de la parthenogenese naturelle. Bulletin Biologique de la France et de la Belgique 62: 164-281. Vrijenhoek RC. 1979. Factors affecting clonal diversity and coexistence. American Zoologist 19: 787-797. _ _.1984. Ecological differentiation among clones: The frozen niche variation model. Pages 217-231 in W6hrmann K, Loescheke V, eds. Population Biology and Evolution. Heidelberg (Germany): SpringerVerlag. ___ .1985. Animal population genetics and disturbance: The effects of local extinctions and recolonizations on heterozygos- www.awl.com/bc I A rich, practical on-line resource for the academic science community 628 ity and fitness. Pages 265-285 in Pickett ST A, White P, eds. The Ecology of Natural Disturbance and Patch Dynamics. New York: Academic Press. ___ . 1989a. Genetic and ecological constraints on the origins and establishment of unisexual vertebrates. Pages 24-31 in Dawley R, Bogart J, eds. Evolution and Ecology of Unisexual Vertebrates. Albany (NY): New York State Museum. Bulletin no. 466. ___ . 1989b. Genotypic diversity and coexistence among sexual and donal forms of Poecifiopsis. Pages 386-400 in Otte D, Endler J, eds. Speciation and Its Consequences. Sunderland (MA): Sinauer Associates. ___ .1990. Genetic diversity and the ecology of asexual populations. Pages 175197 in W6hrmann K, Jain S, eds. Population Biology and Evolution. Berlin (Germany): Springer-Verlag. ___ . 1994. Unisexual fish: Models for studying ecology and evolution. Annual Review of Ecology and Systematics 25: 71-96. Vrijenhoek RC, Pfeiler E. 1997. Differential survival of sexual and asexual Poeciliopsis during environmental stress. Evolution 51: 1593-1600. Vrijenhoek RC, Schultz RJ. 1974. Evolution of a trihybrid unisexual fish (Poeciiiopsis, Poeciliidae). Evolution 28; 306-319. Vrijenhoek RC, Pfeiler E, Wetherington J. 1992. Balancing selection in a desert stream-dwelling fish, Poeciiiopsis monacha. Evolution 46: 1642-1657. Weeks Sc. 1993. The effects of recurrent clonal formation on clonal invasion patterns and sexual persistence: A Monte Carlo simulation of the frozen niche variation model. American Naturalist 141: 409-427. Weeks SC, Gaggiotti OE, Spindler KP, Schenck RE, Vrijenhoek RC. 1992. Feeding behavior in sexual and donal strains of Poeciliopsis. Behavioral Ecology and Sociobiology 30: 1-6. Weider LJ. 1993. A test of the "'generalpurpose" genotype hypothesis: Differential tolerance to thermal and salinity stress among Daphnia clones. Evolution 47: 965-969. WetheringtonJD, Kotora KE, Vrijcnhoek RC. 1987. A test of the spontaneous heterosis hypothesis for unisexual vertebrates. Evolution 41: 721-731. Wetherington JD, Schenck RA, Vrijenhoek RC. 1989a. Origins and ecological success of unisexual Poeciliopsis: The Frozen Niche Variation model. Pages 259-276 in Meffe GA, Snelson Jr. FF, eds. The Ecology and Evolution of Poeciliid Fishes. Englewood Cliffs (NJ): Prentice Hall. Wetherington JD, Weeks SC, Kotora KE, Vrijenhoek RC. 1989b. Genotypic and environmental components of variation in growth and reproduction of fish hemidones (Poeciliopsis: Poeciliidae). Evolution 43: 635-645. White MJD. 1978. Modes of Speciation. San Francisco: W. H. Freeman. Williams Gc. 1975. Sex and Evolution. Princeton (NJ): Princeton University Press. Wright JW, Lowe CH. 1968. Weeds, polyploids, parthenogenesis and the geographical and ecological distribution of all-female species of Cnemidophorus. Copeia 1968: 128-138. BioScience Vol. 48 No.8