Pollen profile,spatial structure,and access to sex in asexual hermaphrodites

Classical cost‐of‐sex models predict the rapid fixation of asexual reproduction. Coexistence of sexuals and asexuals is common among hermaphrodite plants, however, providing asexuals with access to sex via their male function; some of the sexually reproduced progeny they sire will be asexual. The ability of asexuals to sire progeny is often hindered by the production of poor quality pollen. Using cellular automata, it is shown that decreases in pollen quality in asexuals can greatly increase the period of coexistence of sexuals and asexuals and, consequently, the cumulative contribution of sex to asex. Extensive periods of coexistence are only likely, however, if pollen and seed are dispersed locally, in which case coexistence over thousands of generations can be achieved. It is argued that, with local dispersal, the negative relationship between pollen quality and the period of coexistence of sex and asex will result in patterns of geographic parthenogenesis in which asexuals that coexist with sexuals will exhibit a poor male function, whereas asexuals with a very efficient male function will occur in exclusively asexual populations. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 954–966.     

EVOLUTIONARY FEEDBACKS BETWEEN REPRODUCTIVE MODE AND MUTATION RATE EXACERBATE THE PARADOX OF SEX

Evolutionary theory suggests that low mutation rates should favor the persistence of asexuals. Additionally, given the observation that most nonneutral mutations are deleterious, asexuality may strengthen selection for reduced mutation rates. This reciprocal relationship raises the possibility of a positive feedback loop between sex and mutation rate. We explored the consequences of this evolutionary feedback with an individual‐based model in which a sexual population is continually challenged by the introduction of asexual clones. We found that asexuals were more likely to spread in a population when mutation rates were able to evolve relative to a model in which mutation rates were held constant. In fact, under evolving mutation rates, asexuals were able to spread to fixation even when sexuals faced no cost of sex whatsoever. The added success of asexuals was the result of their ability to evolve lower mutation rates and thereby slow the process of mutation accumulation that otherwise limited their spread. Given the existence of ample mutation rate variation in natural populations, our findings show that the evolutionary feedback between sex and mutation rate may intensify the “paradox of sex,” supporting the argument that deleterious mutation accumulation alone is likely insufficient to overcome the reproductive advantage of asexual competitors in the short term.     

Deleterious mutation accumulation in asexual Timema stick insects

Sexual reproduction is extremely widespread in spite of its presumed costs relative to asexual reproduction, indicating that it must provide significant advantages. One postulated benefit of sex and recombination is that they facilitate the purging of mildly deleterious mutations, which would accumulate in asexual lineages and contribute to their short evolutionary life span. To test this prediction, we estimated the accumulation rate of coding (nonsynonymous) mutations, which are expected to be deleterious, in parts of one mitochondrial (COI) and two nuclear (Actin and Hsp70) genes in six independently derived asexual lineages and related sexual species of Timema stick insects. We found signatures of increased coding mutation accumulation in all six asexual Timema and for each of the three analyzed genes, with 3.6- to 13.4-fold higher rates in the asexuals as compared with the sexuals. In addition, because coding mutations in the asexuals often resulted in considerable hydrophobicity changes at the concerned amino acid positions, coding mutations in the asexuals are likely associated with more strongly deleterious effects than in the sexuals. Our results demonstrate that deleterious mutation accumulation can differentially affect sexual and asexual lineages and support the idea that deleterious mutation accumulation plays an important role in limiting the long-term persistence of all-female lineages.     

Can phosphorus limitation contribute to the maintenance of sex? A test of a key assumption

Why sex is so common remains unclear; what is certain is that the predominance of sex despite its profound costs means that it must confer major advantages. Here, we use elemental and nucleic acid assays to evaluate a key element of a novel, integrative hypothesis considering whether sex might be favoured because of differences in body composition between sexuals and asexuals. We found that asexual Potamopyrgus antipodarum, a New Zealand snail, have markedly higher bodily phosphorus and nucleic acid content per unit mass than sexual counterparts. These differences coincide with and are almost certainly linked to the higher ploidy of the asexuals. Our results are the first documented body composition differences between sexual and asexual organisms, and the first detected phenotypic difference between sexual and asexual P. antipodarum, an important natural model system for the study of the maintenance of sex. These findings also verify a central component of our hypothesis that competition between diploid sexuals and polyploid asexuals could be influenced by phosphorus availability.     

Equal fecundity in asexual and sexual mollies (<Emphasis Type="Italic">Poecilia</Emphasis>)

The evolution and maintenance of sexual reproduction is still one of the major unresolved problems in evolutionary biology. Sexual reproduction is fraught with a number of costs as compared to asexual reproduction. For example, sexuals have to produce males, which–given a 1:1 sex ratio—results in a two-fold advantage for asexuals that do not produce males. Consequently, asexuals will outperform and replace sexuals over time assuming everything else is equal. Nonetheless, a few cases of closely related asexuals and sexuals have been documented to coexist stably in natural systems. We investigated the presence of a two-fold cost in a unique system of three closely related fish species: the asexual Amazon Molly (Poecilia formosa), and two sexual species, Sailfin Molly (P. latipinna) and Atlantic Molly (P. mexicana). Amazon Molly reproduce gynogenetically (by sperm dependent parthenogenesis) and always coexist with one of the sexual species, which serves as sperm donor. In the laboratory, we compared reproductive output between P. formosa and P. mexicana as well as P. formosa and P. latipinna. We found no differences in the fecundity in either comparison of a sexual and the asexual species. Under the assumption of a 1:1 sex ratio, the asexual Amazon Molly should consequently have a full two-fold advantage and be able to outcompete sexuals over time. Hence, the coexistence of the species pairs in nature presents a paradox still to be solved.     

Aging asexual lineages and the evolutionary maintenance of sex

Finite populations of asexual and highly selfing species suffer from a reduced efficacy of selection. Such populations are thought to decline in fitness over time due to accumulating slightly deleterious mutations or failing to adapt to changing conditions. These within‐population processes that lead nonrecombining species to extinction may help maintain sex and outcrossing through species level selection. Although inefficient selection is proposed to elevate extinction rates over time, previous models of species selection for sex assumed constant diversification rates. For sex to persist, classic models require that asexual species diversify at rates lower than sexual species; the validity of this requirement is questionable, both conceptually and empirically. We extend past models by allowing asexual lineages to decline in diversification rates as they age, that is nonrecombining lineages “senesce” in diversification rates. At equilibrium, senescing diversification rates maintain sex even when asexual lineages, at young ages, diversify faster than their sexual progenitors. In such cases, the age distribution of asexual lineages contains a peak at intermediate values rather than showing the exponential decline predicted by the classic model. Coexistence requires only that the average rate of diversification in asexuals be lower than that of sexuals.     

The effects of sex and mutation rate on adaptation in test tubes and to mouse hosts by Saccharomyces cerevisiae

Some hypotheses for the evolution of sex focus on adaptation to changing or heterogeneous environments, but these hypotheses have rarely been tested. We tested for advantages of sex and of increased mutation rates in yeast strains in two contrasting environments: a standard and relatively homogeneous laboratory environment of minimal medium in test tubes, and the variable environment of a mouse brain experienced by pathogenic strains. Evolving populations were founded as equal mixtures of sexual and obligately asexual genotypes. In the sexuals, cycles of sporulation, meiosis, and mating were induced approximately every 50 mitotic generations, with the asexuals undergoing sporulation but not ploidy cycles or recombination. In both environments, replicate negative control populations established with the same pair of strains were propagated with neither mating nor meiosis. In test tubes with no sex induced, sexuals were fixed in all five replicates within 250 mitotic generations, whereas in mice with no sex induced, asexuals were fixed in all four replicates by 170 generations. Inducing sex altered these outcomes in opposite directions in test tubes and mice, decreasing the fixation frequencies of sexuals in test tubes but increasing them in mice. These contrasts with asexual controls suggest an advantage for sex in mice but not in test tubes, although there was no difference between test tubes and mice in the numbers of populations fixed-for sexuals. In analogous experiments testing for an advantage of increased mutation rates, wild-type genotypes became fixed at the expense of mutators in every replicate of both test tube and mouse populations, indicating a disadvantage for mutators in both environments. Increased rates of point mutation do not appear to accelerate adaptation.     

Range expansions of sexual versus asexual organisms: Effects of reproductive assurance and migration load

It is generally considered that sexual organisms show faster evolutionary adaptation than asexual organisms because sexuals can accumulate adaptive mutations through recombination. Yet, empirical evidence often shows that the geographic range size of sexual species is narrower than that of closely related asexual species, which may seem as if asexuals can adapt to more varied environments. Two potential explanations for this apparent contradiction considered by the existing theory are reproduction assurance and migration load. Here, we consider both reproductive assurance and migration load within a single model to comparatively examine their effects on range expansions of sexuals and asexuals across an environmental gradient. The model shows that higher dispersal propensity decreases sexuals' disadvantage in reproductive assurance while increasing their disadvantage in migration load. Moreover, lower mutation rate constrains adaptation more strongly in asexuals than in sexuals. Thus, high dispersal propensity and high mutation rates promote that asexuals have wider range sizes than sexuals. Intriguingly, our model reveals that sexuals can have wider geographic range sizes than asexuals under low dispersal propensity and low mutation rates, a pattern consistent with a few exceptional empirical cases. Combining reproductive assurance and migration load provides a useful perspective to better understand the relationships between species' mating systems and their geographic ranges.     

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.     

The cost of males in Daphnia pulex

Sex is paradoxical, because asexuals should replace their sexual ancestors by avoiding the demographic cost of producing males (hereafter referred to as the cost‐of‐males). Despite the large body of theoretical and empirical work dealing with the paradox of sex, the cost‐of‐males assumption has been rarely tested. In the present study, we tested the cost‐of‐males assumption in the cladoceran Daphnia pulex. Populations of this species consist of both cyclically parthenogenetic (i.e. sexuals) and obligately parthenogenetic (i.e. asexuals) lineages. In addition, some of the asexual lineages produce only female offspring, whereas others produce functional males, which can mate with sexual females. We compared the reproductive investment of sexuals, male‐producing asexuals, and non‐male‐producing asexuals when raised separately under various environmental conditions. We also determined the outcome of competition between pair‐wise combinations of these reproductive modes. The cost of males was evident when sexual and asexual females were raised separately: sexuals produced fewer female offspring. However, there was no cost of males when reproductive modes were raised in pairs, as sexuals won the competition with asexuals. Our results directly relate to the field conditions experienced by D. pulex. Sexuals might suffer the cost of males at the beginning of the season, when resource competition is low; but when conditions deteriorate as the population approaches carrying capacity, sexuals seem to be better competitors in spite of male production.     

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.     

Genetic load in sexual and asexual diploids: segregation, dominance and genetic drift

In diploid organisms, sexual reproduction rearranges allelic combinations between loci (recombination) as well as within loci (segregation). Several studies have analyzed the effect of segregation on the genetic load due to recurrent deleterious mutations, but considered infinite populations, thus neglecting the effects of genetic drift. Here, we use single-locus models to explore the combined effects of segregation, selection, and drift. We find that, for partly recessive deleterious alleles, segregation affects both the deterministic component of the change in allele frequencies and the stochastic component due to drift. As a result, we find that the mutation load may be far greater in asexuals than in sexuals in finite and/or subdivided populations. In finite populations, this effect arises primarily because, in the absence of segregation, heterozygotes may reach high frequencies due to drift, while homozygotes are still efficiently selected against; this is not possible with segregation, as matings between heterozygotes constantly produce new homozygotes. If deleterious alleles are partly, but not fully recessive, this causes an excess load in asexuals at intermediate population sizes. In subdivided populations without extinction, drift mostly occurs locally, which reduces the efficiency of selection in both sexuals and asexuals, but does not lead to global fixation. Yet, local drift is stronger in asexuals than in sexuals, leading to a higher mutation load in asexuals. In metapopulations with turnover, global drift becomes again important, leading to similar results as in finite, unstructured populations. Overall, the mutation load that arises through the absence of segregation in asexuals may greatly exceed previous predictions that ignored genetic drift.     

The coevolution of parasites with host-acquired immunity and the evolution of sex

Abstract. Here I present a deterministic model of the coevolution of parasites with the acquired immunity of their hosts, a system in which coevolutionary oscillations can be maintained. These dynamics can confer an advantage to sexual reproduction within the parasite population, but the effect is not strong enough to outweigh the twofold cost of sex. The advantage arises primarily because sexual reproduction impedes the response to fluctuating epistasis and not because it facilitates the response to directional selection—in fact, sexual reproduction often slows the response to directional selection. Where the cost of sexual reproduction is small, a polymorphism can be maintained between the sexuals and the asexuals. A polymorphism is maintained in which the advantage gained due to recombination is balanced by the cost of sex. At much higher costs of sex, a polymorphism between the asexual and sexual populations can still be maintained if the asexuals do not have a full complement of genotypes available to them, because the asexuals only outcompete those sexuals with which they share the same selected alleles. However, over time we might expect the asexuals to amass the full array of genotypes, thus permanently eliminating sexuals from the population. The sexuals may avoid this fate if the parasite population is finite. Although the model presented here describes the coevolution of parasites with the acquired immune responses of their hosts, it can be compared with other host-parasite models that have more traditionally been used to investigate Red Queen theories of the evolution of sex.     

Diversification in sexual and asexual organisms

Abstract Sexual reproduction has long been proposed as a major factor explaining the existence of species and species diversity. Yet, the importance of sex for diversification remains obscure because of a lack of critical theory, difficulties of applying universal concepts of species and speciation, and above all the scarcity of empirical tests. Here, we use genealogical theory to compare the relative tendency of strictly sexual and asexual organisms to diversify into discrete genotypic and morphological clusters. We conclude that asexuals are expected to display discrete clusters similar to those found in sexual organisms. Whether sexuals or asexuals display stronger clustering depends on a number of factors, but in at least some scenarios asexuals should display a stronger pattern. Confounding factors aside, the only explanation we identify for stronger patterns of diversification in sexuals than asexuals is if the faster rates of adaptive change conferred by sexual reproduction promote greater clustering. Quantitative comparisons of diversification in related sexual and asexual taxa are needed to resolve this issue. The answer should shed light not only on the importance of the different stages leading to diversification, but also on the adaptive consequences of sex, still largely unexplored from a macroevolutionary perspective.     

Discordance between nuclear and mitochondrial genomes in sexual and asexual lineages of the freshwater snail Potamopyrgus antipodarum

The presence and extent of mitonuclear discordance in coexisting sexual and asexual lineages provides insight into 1) how and when asexual lineages emerged, and 2) the spatial and temporal scales at which the ecological and evolutionary processes influencing the evolution of sexual and asexual reproduction occur. Here, we used nuclear single‐nucleotide polymorphism (SNP) markers and a mitochondrial gene to characterize phylogeographic structure and the extent of mitonuclear discordance in Potamopyrgus antipodarum. This New Zealand freshwater snail is often used to study the evolution and maintenance of sex because obligately sexual and obligately asexual individuals often coexist. While our data indicate that sexual and asexual P. antipodarum sampled from the same lake population are often genetically similar, suggesting recent origin of these asexuals from sympatric sexual P. antipodarum, we also found significantly more population structure in sexuals vs. asexuals. This latter result suggests that some asexual lineages originated in other lakes and/or in the relatively distant past. When comparing mitochondrial and nuclear population genetic structure, we discovered that one mitochondrial haplotype (‘1A’) was rare in sexuals, but common and widespread in asexuals. Haplotype 1A frequency and nuclear genetic diversity were not associated, suggesting that the commonness of this haplotype cannot be attributed entirely to genetic drift and pointing instead to a role for selection.     

MUTATIONAL MELTDOWNS IN SEXUAL POPULATIONS

Although it is widely acknowledged that the gradual accumulation of mildly deleterious mutations is an important source of extinction for asexual populations, it is generally assumed that this process is of little relevance to sexual species. Here we present results, based on computer simulations and supported by analytical approximations, that indicate that mutation accumulation in small, random-mating monoecious populations can lead to mean extinction times less than a few hundred to a few thousand generations. Unlike the situation in obligate asexuals in which the mean time to extinction (t?_e) increases more slowly than linearly with the population carrying capacity (K), t?_e increases approximately exponentially with K in outcrossing sexual populations. The mean time to extinction for obligately selfing populations is shown to be equivalent to that for asexual populations of the same size, but with half the mutation rate and twice the mutational effect; this suggests that obligate selfing, like obligate asexuality, is inviable as a long-term reproductive strategy. Under all mating systems, the mean time to extinction increases relatively slowly with the logarithm of fecundity, and mutations with intermediate effects (similar to those observed empirically) cause the greatest risk of extinction. Because our analyses ignore sources of demographic and environmental stochasticity, which have synergistic effects that exacerbate the accumulation of deleterious mutations, our results should yield liberal upper bounds to the mean time to extinction caused by mutational degradation. Thus, deleterious mutation accumulation cannot be ruled out generally as a significant source of extinction vulnerability in small sexual populations or as a selective force influencing mating-system evolution.     

The distribution of <Emphasis Type="Italic">F</Emphasis><Subscript><Emphasis Type="Italic">st</Emphasis></Subscript> and other genetic statistics for a class of population structure models

We examine genetic statistics used in the study of structured populations. In a 1999 paper, Wakeley observed that the coalescent process associated with the finite island model can be decomposed into a scattering phase and a collecting phase. This decomposition becomes exact in the large population limit with the coalescent at the end of the scattering phase converging to the Ewens sampling formula and the coalescent during the collecting phase converging to the Kingman coalescent. In this paper we introduce a class of limiting models, which we refer to as G/KC models, that generalize Wakeley’s decomposition. G in G/KC represents a completely general limit for the scattering phase, while KC represents a Kingman coalescent limit for the collecting phase. We show that both the island and two-dimensional stepping stone models converge to G/KC models in the large population limit. We then derive the distribution of the statistic F _st for all G/KC models under a large sample limit for the cases of strong or weak mutation, thereby deriving the large population, large sample limiting distribution of F _st for the island and two-dimensional stepping stone models as a special case of a general formula. Our methods allow us to take the large population and large sample limits simultaneously. In the context of large population, large sample limits, we show that the variance of F _st in the presence of weak mutation collapses as O(\frac1logd){O(\frac{1}{\log d})} where d is the number of demes sampled. Further, we show that this O(\frac1logd){O(\frac{1}{\log d})} is caused by a heavy tail in the distribution of F _st . Our analysis of F _st can be extended to an entire class of genetic statistics, and we use our approach to examine homozygosity measures. Our analysis uses coalescent based methods.     

THE GENETIC STRUCTURE OF A GYNODIOECIOUS PLANT: NUCLEAR AND CYTOPLASMIC GENES

Sex expression in gynodioecious plants is often determined by an interaction between biparentally and maternally inherited genes. Their relative rates of gene flow should be considered when modeling the evolution of the sex ratio in structured populations. In order to understand patterns of gene flow in Silene vulgaris, a gynodioecious plant, genetic structure was estimated from biparentally inherited genetic markers (allozymes) and a maternally inherited marker (chloroplast DNA) using Wright's F_st. Based on data from 16 local populations, chloroplast DNA showed considerably more genetic structure than did allozymes (F_st values of 0.62 and 0.22, respectively). This suggests that the rate of gene flow is about three times greater for nuclear genes.     

Novel distribution pattern between coexisting sexual and obligate asexual variants of the true estuarine macroalga Ulva prolifera

Where sexual and asexual forms coexist within a species, the asexuals are often found to be prevalent in marginal habitats. This asexual distribution pattern has received evolutionary attention linked to the paradox of sex. In many marine species, there is a distributional trend of asexual modes being more common in lower salinity waters regarded as the ecogeographic marginal, being explained by negative effects of low salinities on sexual reproductive success. However, the distribution pattern of estuarine species recently adapted to low salinity waters has remained unknown. The brackish macroalga Ulva prolifera being a major benthic component of estuarine ecosystems includes a sexual variant and obligate asexual variants by means of motile spores. We examined the sexual–asexual distribution pattern of this alga along a salinity gradient in river estuaries. Surprisingly, opposite to the distributional trend of marine organisms, the results clearly showed the persistent predominance of sexuals in the lower salinity reaches than the asexuals. In addition, a frequent alternating of dioecious gametophytes and sporophytes in the sexual population was observed, suggesting the sexual reproductive process would be robustly performed in the low salinity waters. Considering U. prolifera had evolved from the ancestral marine species to become a true estuarine species of which the core habitat is the low salinity reaches, in a broad sense its sexual–asexual distribution pattern would be involved in asexual marginal occupations of the species range previously reported in other organisms. Based on the frozen niche variation model, we can give a concise explanation for the evolutionary process of this pattern; multiple asexuals with frozen genotypic variation had arisen from sexual ancestors undergoing low salinity adaptation and share the estuarine habitat with the sexuals at present.     

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.