EXPERIMENTAL STUDIES OF THE EVOLUTIONARY SIGNIFICANCE OF SEXUAL REPRODUCTION. V. A FIELD TEST OF THE SIB-COMPETITION LOTTERY HYPOTHESIS

Sexually and asexually derived tillers of Anthoxanthum odoratum were planted directly in the field to test the hypothesis that competition among groups of sexual and asexual siblings favors the maintenance of sexual reproduction in populations. The results showed a substantial fitness advantage for sexual tillers. However, in contrast with the models, the advantage of sex did not increase with increasing numbers of colonists in the patch, there were multiple survivors among colonists, and an advantage was observed even for singly planted tillers. When a truncation-selection scheme was imposed ex post facto on the data, the relative performance of sexual tillers was similar to that predicted by the Bulmer (1980) model, suggesting that sib-competition models fail due to the violation of the assumption of truncation selection. The advantage of sex was not correlated with the presence of other species, total percentage cover, or species diversity, although sites where sex was favored were physically clustered.     

ENVIRONMENTAL STRESS AND THE MAINTENANCE OF SEX IN A FRESHWATER SNAIL

Synergism among mutations can lead to an advantage to sexual reproduction, provided mutation rates are high enough (the mutational deterministic hypothesis). Here we tested the idea that competition for food can increase the advantage to sexual reproduction, perhaps by increasing the synergism among mutations in asexual individuals. We compared the survivorship of sexual and asexual snails (Potamopyrgus antipodarum) under two treatments: starved and fed. We predicted higher mortality for asexual snails when starved, but found that sexual and asexual individuals survived at the same rate, independent of treatment. These results suggest that the distribution of sex in this snail may not be explained by variation in competition among populations.     

EXPERIMENTAL STUDIES OF THE EVOLUTIONARY SIGNIFICANCE OF SEXUAL REPRODUCTION II. A TEST OF THE DENSITY-DEPENDENT SELECTION HYPOTHESIS

This study tests the hypothesis that one evolutionary advantage of sexual reproduction is that it produces genetically variable progeny with a density-dependent advantage mediated by resource partitioning or pest pressure. Our experimental approach involved planting separate plots of sexually-derived and asexually-derived tillers of the grass Anthoxanthum odoratum in density gradients at the two natural sites from which the source material was taken. The sexual progeny displayed a significant fitness advantage compared to the asexual progeny. But, in contrast to the expectations of the density-dependent selection hypothesis, the advantage of the sexually produced progeny is most marked at lower densities. Thus, the results of this experiment and our previous report (Antonovics and Ellstrand, 1984) seem to best support the frequency-dependent selection hypothesis for the advantage of sexual reproduction.     

ON THE COEXISTENCE AND COEVOLUTION OF ASEXUAL AND SEXUAL COMPETITORS

The coexistence and coevolution of sexual and asexual species under resource competition are explored with three models: a nongenetic ecological model, a model including single locus genetics, and a quantitative-genetic model. The basic assumption underlying all three models is that genetic differences are translated into ecological differences. Hence if sexual species are genetically more variable, they will be ecologically more variable. Under classical competition theory, this increased ecological variability can, in many cases, be an advantage to individual sexual genotypes and to the sexual species as a whole. The purpose of this paper is to determine the conditions when this advantage will outway three disadvantages of sexuality: the costs of males, of segregation, and of the additive component of recombination. All three models reach similar conclusions. Although asexuality confers an advantage, it is much less than a two-fold advantage because minor increases in the overall species niche width of the sexual species will offset the reproductive advantage of the asexual species. This occurs for two reasons. First, an increase in species niche width increases the resource base of the sexual species. Second, to the extent that the increase in niche width is due to increased differences between individuals, a reduction in intraspecific competition will result. This is not to imply that the sexual species will always win. The prime conditions that enable sexual species to stably coexist with or even supplant an asexual sister species are:

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THE DISTRIBUTION OF LIFE-HISTORY VARIATION IN THE DAPHNIA PULEX COMPLEX

In the midwestern United States the Daphnia pulex complex consists of a mosaic of sexual and asexual populations, providing a useful model system for studying the evolutionary forces underlying the maintenance of sex. One asexual and two sexual populations were surveyed for genetic variation for isozymes, mitochondrial DNA, and life-history characters. While the sexual populations exhibited substantial levels of genetic variance for fitness characters, no variation was detected in the asexual population at any level. However, a parallel survey among asexual clones derived from other ponds revealed large amounts of quantitative variation among clones, even among those with the same molecular profile. As a group, the asexuals are more variable for life histories than are the sexual populations. The molecular data indicate a relatively recent origin for the extant asexual D. pulex. The polyphyletic origin of these clones, combined with their microevolutionary potential, provides an explanation for their broad geographic distribution. The distribution of sex in the complex cannot be explained with the standard models that assume an invariant asexual population in reproductive isolation from the parental species. Although the frequency of asexuality may be driven by the spread of a sex-limited meiosis suppressor through sexual populations, the complete displacement of sexuality may be prevented by ecological distinctions between the two classes of individuals. On average, the asexuals are larger but produce smaller clutches than the sexuals.     

EVOLUTION OF ASEXUALITY IN THE COSMOPOLITAN MARINE CLAM LASAEA

The marine clam genus Lasaea is unique among marine bivalves in that it contains both sexual and asexual lineages. We employed molecular tools to infer intrageneric relationships of geographically restricted sexual versus cosmopolitan asexual forms. Polymerase chain reaction primers were used to amplify and sequence homologous 624 nucleotide fragments of COIII from polyploid, asexual, direct-developing individuals representing northeastern Pacific, northeastern Atlantic, Mediterranean, southern Indian Ocean, and Australian populations. DNA sequences also were obtained from the two known diploid congeners, the Australian sexual, indirect developer, Lasaea australis, and an undescribed meiotic Australian direct developer. Estimated tree topologies did not support monophyly for polyploid asexual Lasaea lineages. A robust dichotomy was evident in all phylogenetic trees and each of the two main branches included one of the diploid meitoic Australian congeners. Lasaea australis clustered with two of the direct-developing, polyploid asexual haplotypes, one from Australia, the other from the northeastern Atlantic. Monophyly is supported for the diploid Australian direct-developing lineage together with the remaining polyploid asexual lineages from the northeastern Pacific, northeastern Atlantic, Mediterranean, and southern Indian Ocean. These results indicate that asexual Lasaea lineages are polyphyletic and may have resulted from multiple hybridization events. The high degree of genetic divergence of asexual lineages from co-clustering meiotic congeners (16%–22%) and among geographically restricted monophyletic clones (9%–11%) suggests that asexual Lasaea lineages may be exceptionally long lived.     

ON GENETIC SEGREGATION AND THE EVOLUTION OF SEX

It has recently been argued that because the genetic load borne by an asexual species resulting from segregation, relative to a comparable sexual population, is greater than two, sex can overcome its twofold disadvantage and succeed. We evaluate some of the assumptions underlying this argument and discuss alternative assumptions. Further, we simulate the dynamics of competition between sexual and asexual types. We find that for populations of size 100 and 500 the advantages of segregation do not outweigh the cost of producing males. We conclude that, at least for small populations, drift and the cost of sex govern the evolution of sexuality, not selection or segregation. We believe, however, that if sexual and asexual populations were isolated for a sufficiently long period, segregation might impart a fitness advantage upon sexuals that could compensate for the cost of sex and allow sexuals to outcompete asexuals upon their reunion.     

THE MAINTENANCE OF SEX BY GROUP SELECTION

The traditional group-selection model for the maintenance of sex is based upon the assumption that the long-term evolutionary benefits of sexual reproduction result in asexual lineages having a higher extinction rate than sexual species. This model is reexamined, as is a related model that incorporates the possibility that sexual and asexual lines differ in their speciation rates. In these models, the long-term advantage of sex is opposed by a strong short-term disadvantage arising from the twofold reproductive cost of producing males. It is shown that once some sexual lines become established, then group selection can act to maintain sex despite its short-term disadvantage. The short-term disadvantage is included in the model by assuming that, if asexual individuals arise by mutation within a previously completely sexual species, then the asexuals quickly displace their sexual conspecifics and the species is transformed to asexuality. The probability of this event is given by the transition rate, u_s. If the value of u_s varies between lineages, then one of the effects of group selection is to favor groups (i.e., species) with the lowest values of u_s. This occurs because lines that do convert to asexuality (because of a high u_s) are doomed to a high rate of extinction, and in the long term only those that do not convert to asexuality (because of a low u_s) survive. The net result of group selection is that sex is maintained because of its lower extinction rate (or higher speciation rate) and because asexual mutants only rarely arise.     

Can punishment maintain sex?

Individuals who reproduce asexually have a two-fold advantage over their sexually-reproducing counterparts as they are able to reproduce twice as fast. Explaining why sexual reproduction is favoured over asexual reproduction therefore remains an important challenge in evolutionary biology. Various mechanisms involving resistance to parasites, adaptation to novel environments and helping to purge the genome of deleterious mutations have all been proposed as potential mechanisms which could promote the evolution of sex. A recent article has suggested that spiteful males may help to reduce the two-fold advantage of asexual females. Here I discuss this idea, and further ask whether punishment of asexual females by sexual females could be one way in which sexual reproduction could be maintained in groups of animals; in light of recent research on the repression of competition, it could be possible that asexual females which reproduce faster than their sexual counterparts will be punished for using group resources. It may therefore be possible that the behaviour of sexual individuals towards asexual females could have fitness consequences which could potentially reduce the two-fold advantage they gain from reproducing parthenogenetically.     

THE GENETIC STRUCTURE OF LARGE-LAKE DAPHNIA POPULATIONS

Cyclical parthenogenesis allows study of the genetic and evolutionary characteristics of groups exhibiting both asexual and sexual reproduction. The cladoceran genus Daphnia contains species which vary with respect to the relative incidence of sexual reproduction; pond species tend to undergo sexual reproduction more regularly than species found in large lakes. Previous genetic studies have focused on pond populations, generating expectations about large-lake populations that have not been fully met by recent studies. The present study of the Palearctic species Daphnia galeata further examines the genetic structure of large-lake populations. Nine local populations, from lakes in northern Germany, are examined for genetic variation at seven enzyme loci. Populations exhibit similar allelic arrays and often similar allele frequencies at the five polymorphic loci; values of Nei's genetic distance (D) ranged from 0.002 to 0.239, with a mean of 0.084. F_ST values range from 0.012 to 0.257, and spatial autocorrelation coefficients range from -0.533 to 0.551, for the eight alleles analyzed. With few exceptions, within-population genotypic frequencies were in Hardy-Weinberg equilibrium. There was, however, significant heterogeneity in genotypic frequencies among populations. The number of coexisting clonal groups, as determined by three locus genotypes, is high within populations. Clonal groups are widely distributed among localities. The amount of genetic divergence observed among these large-lake populations is smaller than that previously observed among pond populations and suggests that different processes may be important in determining the genetic structure and subsequent phenotypic divergence of lake versus pond populations.     

Parasite resistance predicts fitness better than fecundity in a natural population of the freshwater snail Potamopyrgus antipodarum

The cost of males should give asexual females an advantage when in competition with sexual females. In addition, high‐fecundity asexual genotypes should have an advantage over low‐fecundity clones, leading to reduction in clonal diversity over time. To evaluate fitness components in a natural population, we measured the annual reproductive rate of individual sexual and asexual female Potamopyrgus antipodarum, a New Zealand freshwater snail, in field enclosures that excluded competitors and predators. We used allozyme genotyping to assign the asexual females to particular clonal genotypes. We found that the most fecund asexual clones had similar or higher fecundity as the top 10% of sexual families, suggesting that fecundity selection, even without the cost of males, would lead to replacement of the sexual population by clones. Consequently, we expected that the clones with the highest fecundity would dominate the natural population. Counter to this prediction, we found that high annual reproductive rates did not correlate with the frequency of clones in the natural population. When we exposed the same clones to parasites in the laboratory, we found that resistance to infection was positively correlated with the frequency of clones in the population. The correlation between fecundity and parasite resistance was negative, suggesting a trade‐off between these two traits. Our results thus suggest that parasite resistance is an important short‐term predictor of the success of asexual P. antipodarum in this population.     

EVOLUTION OF TRADE-OFFS BETWEEN SEXUAL AND ASEXUAL PHASES AND THE ROLE OF REPRODUCTIVE PLASTICITY IN THE GENETIC ARCHITECTURE OF APHID LIFE HISTORIES

Life‐history theory postulates that evolution is constrained by trade‐offs (i.e., negative genetic correlations) among traits that contribute to fitness. However, in organisms with complex life cycles, trade‐offs may drastically differ between phases, putatively leading to different evolutionary trajectories. Here, we tested this possibility by examining changes in life‐history traits in an aphid species that alternates asexual and sexual reproduction in its life cycle. The quantitative genetics of reproductive and dispersal traits was studied in 23 lineages (genotypes) of the bird cherry‐oat aphid Rhopalosiphum padi, during both the sexual and asexual phases, which were induced experimentally under specific environmental conditions. We found large and significant heritabilities (broad‐sense) for all traits and several negative genetic correlations between traits (trade‐offs), which are related to reproduction (i.e., numbers of the various sexual or asexual morphs) or dispersal (i.e., numbers of winged or wingless morphs). These results suggest that R. padi exhibits lineage specialization both in reproductive and dispersal strategies. In addition, we found important differences in the structure of genetic variance–covariance matrices ( G ) between phases. These differences were due to two large, negative genetic correlations detected during the asexual phase only: (1) between fecundity and age at maturity and (2) between the production of wingless and winged parthenogenetic females. We propose that this differential expression in genetic architecture results from a reallocation scheme during the asexual phase, when sexual morphs are not produced. We also found significant G × E interaction and nonsignificant genetic correlations across phases, indicating that genotypes could respond independently to selection in each phase. Our results reveal a rather unique situation in which the same population and even the same genotypes express different genetic (co)variation under different environmental conditions, driven by optimal resource allocation criteria.     

POLYPHYLETIC ORIGINS OF ASEXUALITY IN DAPHNIA PULEX. I. BREEDING-SYSTEM VARIATION AND LEVELS OF CLONAL DIVERSITY

There is growing evidence that transitions from sexual to asexual reproduction are often provoked by internal genetic factors rather than extrinsic selection pressures. In the cladoceran crustacean Daphnia pulex, the shift to asexuality has been linked to sex-limited meiosis suppression. Most populations of this species reproduce by obligate parthenogenesis, but cyclically parthenogenetic populations persist in the southern portion of its range. The meiosis-suppressor model predicts that asexuality in D. pulex has polyphyletic origins and that the coexistence of cyclically parthenogenetic lines with male-producing obligately asexual clones should be unstable. For the present study, we examined the genotypic structure of D. pulex populations from a region in which there is an abrupt microgeographical shift in breeding system. Populations in Michigan largely reproduce by cyclic parthenogenesis, while those in Ontario are obligately asexual. Allozyme studies on 77 populations from this area revealed 50 obligately asexual clones, divisible into two groups: one derived from a single parent species and the other derived via interspecific hybridization. Although nearly 50% of the clones retained male production, there was, as predicted, no evidence of coexistence between cyclically parthenogenetic populations and male-producing obligately asexual clones. The survey did, however, reveal a low incidence of cyclically parthenogenetic populations in Ontario. The high genotypic diversity of these populations suggests that they are not only resistant to meiosis suppression, but able to rework genetic variation gained from asexual clones into a sexual breeding system.     

VARIATION IN THE STRENGTH OF MALE MATE CHOICE ALLOWS LONG‐TERM COEXISTENCE OF SPERM‐DEPENDENT ASEXUALS AND THEIR SEXUAL HOSTS

In several asexual taxa, reproduction requires mating with related sexual species to stimulate egg development, even though genetic material is not incorporated from the sexuals (gynogenesis). In cases in which gynogens do not invest in male function, they can potentially have a twofold competitive advantage over sexuals because the asexuals avoid the cost of producing males. If unmitigated, however, the competitive success of the asexuals would ultimately lead to their own demise, following the extinction of the sexual species that stimulate egg development. We have studied a model of mate choice among sexual individuals and asexual gynogens, where males of the sexual species preferentially mate with sexual females over gynogenetic females, to determine if such mating preferences can stably maintain both gynogenetic and sexual individuals within a community. Our model shows that stable coexistence of gynogens and their sexual hosts can occur when there is variation among males in the degree of preference for mating with sexual females and when pickier males pay a higher cost of preference.     

Why reproduce sexually?

There is reason to believe that intense selection, such that only a small minority at the top of the fitness distribution has any appreciable chance of survival, can sometimes give sexual reproduction an immediate (one-life-cycle) advantage over asexual. The advantage must be great enough to balance the 50% loss of genetic material in meiosis.One model shows the advantage to be frequency-dependent in life cycles in which there are several asexual generations and one sexual. The observed frequency of sexual reproduction in such a life cycle is explained as an evolutionary equilibrium by this model. In another model the optimum frequency of asexual reproduction drops to zero as fecundity and competition increase. This explains the exclusively sexual reproduction of such fecund organism as elms and oysters. Once lost, asexual reproduction may be difficult to evolve secondarily. This explains the presence of such exclusively sexual, low-fecundity organisms as the higher vertebrates.     

Genetics of decayed sexual traits in a parasitoid wasp with endosymbiont-induced asexuality

Trait decay may occur when selective pressures shift, owing to changes in environment or life style, rendering formerly adaptive traits non-functional or even maladaptive. It remains largely unknown if such decay would stem from multiple mutations with small effects or rather involve few loci with major phenotypic effects. Here, we investigate the decay of female sexual traits, and the genetic causes thereof, in a transition from haplodiploid sexual reproduction to endosymbiont-induced asexual reproduction in the parasitoid wasp Asobara japonica. We take advantage of the fact that asexual females cured of their endosymbionts produce sons instead of daughters, and that these sons can be crossed with sexual females. By combining behavioral experiments with crosses designed to introgress alleles from the asexual into the sexual genome, we found that sexual attractiveness, mating, egg fertilization and plastic adjustment of offspring sex ratio (in response to variation in local mate competition) are decayed in asexual A. japonica females. Furthermore, introgression experiments revealed that the propensity for cured asexual females to produce only sons (because of decayed sexual attractiveness, mating behavior and/or egg fertilization) is likely caused by recessive genetic effects at a single locus. Recessive effects were also found to cause decay of plastic sex-ratio adjustment under variable levels of local mate competition. Our results suggest that few recessive mutations drive decay of female sexual traits, at least in asexual species deriving from haplodiploid sexual ancestors.     

THE ORIGIN AND DISTRIBUTION OF CLONAL DIVERSITY IN ALSOPHILA POMETARIA (LEPIDOPTERA: GEOMETRIDAE)

A survey of spatial and temporal variation in the frequency of electrophoretically defined genotypes in the geometrid moth Alsophila pometaria revealed a high diversity of uncommon or rare asexual genotypes and clinal distributions of two of the more common clones. There was substantial year-to-year variation in genotype frequencies in seven of eleven sites. Progeny tests have revealed that sexual reproduction is uncommon in two populations and that new asexual genotypes arise from the sexual population. The recurrent origin of asexual genotypes is likely to account for the high genetic and ecological diversity of the asexual contingent of this species' populations, in contrast to the lower genetic diversity in some obligately asexual species in which such recruitment does not occur.     

INTERPOPULATIONAL VARIATION IN THE GAMETOPHYTES OF PELLAEA ANDROMEDAEFOLIA

The development and mature morphology of the gametophytes from both sexual and apogamous populations of the fern Pellaea andromedaefolia were investigated. While most sexual examples were indistinguishable, some differences were noted. An insular collection was distinctive in its variability and irregularity of form. Although the latter was a representative of var. pubescens, other collections of the variety could not be distinguished from var. andromedaefolia on the basis of gametophytic characteristics. The apogamous gametophytes were decidedly more variable in development and often very different from sexual thalli. The mature asexual thalli tended to be more irregular in form and usually sharply divergent from the typical cordate type characteristic of the sexual populations. Each of the five apogamous samples was unique with respect to gametophyte development. The differences among the gametophytes of the various populations do not correlate with the sporophytic characteristics which differentiate the two varieties of the species.     

LARGE POPULATION SIZE PREDICTS THE DISTRIBUTION OF ASEXUALITY IN SCALE INSECTS

Understanding why some organisms reproduce by sexual reproduction while others can reproduce asexually remains an important unsolved problem in evolutionary biology. Simple demography suggests that asexuals should outcompete sexually reproducing organisms, because of their higher intrinsic rate of increase. However, the majority of multicellular organisms have sexual reproduction. The widely accepted explanation for this apparent contradiction is that asexual lineages have a higher extinction rate. A number of models have indicated that population size might play a crucial role in the evolution of asexuality. The strength of processes that lead to extinction of asexual species is reduced when population sizes get very large, so that the long‐term advantage of sexual over asexual reproduction may become negligible. Here, we use a comparative approach using scale insects (Coccoidea, Hemiptera) to show that asexuality is indeed more common in species with larger population density and geographic distribution and we also show that asexual species tend to be more polyphagous. We discuss the implication of our findings for previously observed patterns of asexuality in agricultural pests.     

Resource competition between genetically varied and genetically uniform populations of Daphnia pulex (Leydig): does sexual reproduction confer a short‐term ecological advantage?

Small competitive advantages may suffice to compensate for a large disadvantage in intrinsic growth capacity. This well‐known principle from ecology has recently been applied to the enduring question of how sexual reproduction can persist in the face of invasion by female‐only parthenogens. Small competitive advantages resulting directly from sexual reproduction are predicted to cancel a two‐fold disadvantage in intrinsic growth capacity caused by males (which do not themselves produce offspring) comprising half the sexual population. In this paper we test the principal assumption of this theory, that the genetic variation produced by sexual reproduction confers a competitive advantage over self‐identical asexual invaders. We set up competition between a diverse clonal assembly of Daphnia pulex and genetically uniform populations from single clones. At young ages, the population comprising genetically varied Daphnia had significantly higher birth rates in competition with populations of genetically uniform Daphnia than in competition with itself, indicating competitive release and a Lotka–Volterra competition coefficient α₁₂ < 1. No such difference was apparent under conditions of greater food stress, possibly due to individuals channelling more energy into survival, or for old‐aged populations, possibly as a result of reduced selective pressures for high reproduction in old females. Mean birth rates differed between the clones at all ages in the presence of competition, providing evidence of variation in life history traits between clones. A Lotka–Volterra model predicted empirical estimates of α₁₂ = 0.896 (genetically uniform on varied) and α₂₁ = 1.010 (varied on uniform), which permits immediate coexistence of a sexual population of D. pulex even with an asexual lineage having twice the intrinsic growth capacity. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85 , 111–123.