PARTHENOGENESIS IN A FRESHWATER SNAIL: REPRODUCTIVE ASSURANCE VERSUS PARASITIC RELEASE

Two alternative (but not mutually exclusive) hypotheses were contrasted for their abilities to explain the distribution of parthenogenesis in the freshwater snail Potamopyrgus antipodarum: the reproductive assurance hypothesis, which predicts that parthenogenesis will be favored in sparse populations where mates are difficult to find, and the Red Queen hypothesis, which predicts that parthenogenesis will be favored in populations that have a low risk of parasitism. The results were inconsistent with the prediction of the reproductive assurance hypothesis; male frequency was not significantly or positively correlated with snail density. Thus, there was no support for any of the hypotheses for the maintenance of sex that rely on selection for reproductive assurance to explain the distribution of parthenogenesis (e.g., recombinational repair). The results, however, were consistent with the Red Queen hypothesis; male frequency was positively and significantly correlated with the frequency of individuals infected by trematodes. This correlation suggests that parthenogenetic females have replaced sexual females in populations where parasites are rare, and that sexual females have persisted in populations where parasites are common.     

Bloody‐minded parasites and sex: the effects of fluctuating virulence

Asexual lineages can grow at a faster rate than sexual lineages. Why then is sexual reproduction so widespread? Much empirical evidence supports the Red Queen hypothesis. Under this hypothesis, coevolving parasites favour sexual reproduction by adapting to infect common asexual clones and driving them down in frequency. One limitation, however, seems to challenge the generality of the Red Queen: in theoretical models, parasites must be very virulent to maintain sex. Moreover, experiments show virulence to be unstable, readily shifting in response to environmental conditions. Does variation in virulence further limit the ability of coevolving parasites to maintain sex? To address this question, we simulated temporal variation in virulence and evaluated the outcome of competition between sexual and asexual females. We found that variation in virulence did not limit the ability of coevolving parasites to maintain sex. In fact, relatively high variation in virulence promoted parasite‐mediated maintenance of sex. With sufficient variation, sexual females persisted even when mean virulence fell well below the threshold virulence required to maintain sex under constant conditions. We conclude that natural variation in virulence does not limit the relevance of the Red Queen hypothesis for natural populations; on the contrary, it could expand the range of conditions over which coevolving parasites can maintain sex.     

Sex differences in host defence interfere with parasite‐mediated selection for outcrossing during host–parasite coevolution

The Red Queen hypothesis proposes that coevolving parasites select for outcrossing in the host. Outcrossing relies on males, which often show lower immune investment due to, for example, sexual selection. Here, we demonstrate that such sex differences in immunity interfere with parasite‐mediated selection for outcrossing. Two independent coevolution experiments with Caenorhabditis elegans and its microparasite Bacillus thuringiensis produced decreased yet stable frequencies of outcrossing male hosts. A subsequent systematic analysis verified that male C. elegans suffered from a direct selective disadvantage under parasite pressure (i.e. lower resistance, decreased sexual activity, increased escape behaviour), which can reduce outcrossing and thus male frequencies. At the same time, males offered an indirect selective benefit, because male‐mediated outcrossing increased offspring resistance, thus favouring male persistence in the evolving populations. As sex differences in immunity are widespread, such interference of opposing selective constraints is likely of central importance during host adaptation to a coevolving parasite.     

Faster clonal turnover in high‐infection habitats provides evidence for parasite‐mediated selection

According to the Red Queen hypothesis for sex, parasite‐mediated selection against common clones counterbalances the reproductive advantage of asexual lineages, which would otherwise outcompete sexual conspecifics. Such selection on the clonal population is expected to lead to a faster clonal turnover in habitats where selection by parasites is stronger. We tested this prediction by comparing the genetic structure of clonal and sexual populations of freshwater snail Potamopyrgus antipodarum between years 2003 and 2007 in three depth‐specific habitats in Lake Alexandrina (South Island, New Zealand). These habitats differ in the risk of infection by castrating trematodes and in the relative proportion of sexual individuals. As predicted, we found that the clonal structure changed significantly in shallow and mid‐water habitats, where prevalence of infection was high, but not in the deep habitat, where parasite prevalence was low. Additionally, we found that both clonal diversity and evenness of the asexual population declined in the shallow habitat. In contrast, the genetic structure (based on F–statistics) of the coexisting sexual population did not change, which suggests that the change in the clonal structure cannot be related to genetic changes in the sexual population. Finally, the frequency of sexuals had no effect on the diversity of the sympatric clonal population. Taken together, our results show a more rapid clonal turnover in high‐infection habitats, which gives support for the Red Queen hypothesis for sex.     

Parthenogenetic vs. sexual reproduction in oribatid mite communities

The dominance of sex in Metazoa is enigmatic. Sexual species allocate resources to the production of males, while potentially facing negative effects such as the loss of well‐adapted genotypes due to recombination, and exposure to diseases and predators during mating. Two major hypotheses have been put forward to explain the advantages of parthenogenetic versus sexual reproduction in animals, that is, the Red Queen hypothesis and the Tangled Bank/Structured Resource Theory of Sex. The Red Queen hypothesis assumes that antagonistic predator—prey/ parasite–host interactions favor sex. The Structured Resource Theory of Sex predicts sexual reproduction to be favored if resources are in short supply and aggregated in space. In soil, a remarkable number of invertebrates reproduce by parthenogenesis, and this pattern is most pronounced in oribatid mites (Oribatida, Acari). Oribatid mites are abundant in virtually any soil across very different habitats, and include many sexual and parthenogenetic (thelytokous) species. Thereby, they represent an ideal model group to investigate the role of sexual versus parthenogenetic reproduction across different ecosystems and habitats. Here, we compiled data on oribatid mite communities from different ecosystems and habitats across biomes, including tropical rainforests, temperate forests, grasslands, arable fields, salt marshes, bogs, caves, and deadwood. Based on the compiled dataset, we analyzed if the percentage of parthenogenetic species and the percentage of individuals of parthenogenetic species are related to total oribatid mite density, species number, and other potential driving factors of the reproductive mode including altitude and latitude. We then interpret the results in support of either the Red Queen hypothesis or the Structured Resource Theory of Sex. Overall, the data showed that low density of oribatid mites due to harsh environmental conditions is associated with high frequency of parthenogenesis supporting predictions of the Structured Resource Theory of Sex rather than the Red Queen hypothesis.     

Parasites, sex, and clonal diversity in natural snail populations

Under the Red Queen hypothesis, host-parasite coevolution selects against common host genotypes. Although this mechanism might underlie the persistence of sexual reproduction, it might also maintain high clonal diversity. Alternatively, clonal diversity might be maintained by multiple origins of parthenogens from conspecific sexuals, a feature in many animal groups. Herein, we addressed the maintenance of overall genetic diversity by coevolving parasites, as predicted by the Red Queen hypothesis. We specifically examined the contribution of parasites to host clonal diversity and the frequency of sexually reproducing individuals in natural stream populations of Potamopyrgus antipodarum snails. We also tested the alternative hypothesis that clonal diversity is maintained by the input of clones by mutation from sympatric sexuals. Clonal diversity and the frequency of sexual individuals were both positively related to infection frequency. Surprisingly, although clones are derived by mutation from sexual snails, parasites explained more of the genotypic variation among parthenogenetic subpopulations. Our findings thus highlight the importance of parasites as drivers of clonal diversity, as well as sex.     

Geographic variation in sterilizing parasite species and the Red Queen

The Red Queen hypothesis predicts that sexual reproduction should be favoured in locations where the risk of infection by virulent parasites is consistently high. When hosts are exposed to multiple parasites over their geographic range, the coevolving parasite species may vary among host populations. We surveyed 26 streams on the South Island of New Zealand to determine whether the frequency of snails ( Potamopyrgus antipodarum ) infected by various sterilizing trematode parasite species was correlated with the frequency of sexual individuals. We compared the results with a survey conducted over 20 years ago to determine whether the associations were consistent. We also evaluated different measures of parasite-mediated selection among populations, including prevalence of the most common local parasite (MCLP) species and parasite diversity to assess the best predictor of sexual reproduction among stream populations. The results showed that the relationship between male frequency and parasite infection is more geographically widespread than previously recorded. Additionally, we found that the prevalence of the MCLP was the best predictor of sex in habitats where hosts populations are infected with multiple parasites (approximately 15 trematode species). This study provides evidence that sexual snails occur more often in environments with high infection levels, and that the pattern of parasite-imposed selection is geographically variable. Support for the Red Queen may be strengthened by focussing on the MCLP, which may vary among host populations.     

On sex, mate selection and the red queen.

The widespread occurrence of sexual reproduction despite the two-fold disadvantage of producing males, is still an unsolved mystery in evolutionary biology. One explanatory theory, called the "Red Queen" hypothesis, states that sex is an adaptation to escape from parasites. A more recent hypothesis, the mate selection hypothesis, assumes that non-random mating, possible only with sex, accelerates the evolution of beneficial traits. This paper tests these two hypotheses, using an agent-based or "micro-analytic" evolutionary algorithm where host-parasite interaction is simulated adhering to biological reality. While previous simpler models testing the "Red Queen" hypothesis considered mainly haploid hosts, stable population density, random mating and simplified expression of fitness, our more realistic model allows diploidy, mate selection, live history constraints and variable population densities. Results suggest that the Red Queen hypothesis is not valid for more realistic evolutionary scenarios and that each of the two hypotheses tested seem to explain partially but not exhaustively the adaptive value of sex. Based on the results we suggest that sexual populations in nature should avoid both, maximizing outbreeding or maximizing inbreeding and should acquire mate selection strategies which favour optimal ranges of genetic mixing in accordance with environmental challenges.     

Major histocompatibility complex variability in the clonal Amazon molly,Poecilia formosa: is copy number less important than genotype?

The evolution of sex is still a major unsolved puzzle in biology. One of the most promising theoretical models to answer this question is the Red Queen hypothesis. The Red Queen hypothesis proposes a fast adaptation of pathogens to common genotypes and therefore a negative frequency-dependent selection against common genotypes. Clonal organisms should be especially endangered when co-occurring with closely related sexual species. In this context, major histocompatibility (MHC) genes have been discussed to be auspicious candidates that could provide the genetic basis on which selection for immune competence could act. In this study, we investigated MHC variability in a clonal teleost fish: the Amazon molly, Poecilia formosa . The Amazon molly is an ideal candidate to test the Red Queen hypothesis as it is a clonal species but co-occurs with a closely related sexual species and should therefore be especially susceptible to pathogen infection. We found that allele numbers did in general not differ between sexual and clonal 'species' but that genotypic variability is reduced in the clonally reproducing fish, especially in the polyploids. We conclude that in clonal organisms, genotype frequency might be more important for immune competence than MHC allele number. Amazon mollies and their co-occurring parental species clearly fulfil a prerequisite of the Red Queen hypothesis and should therefore provide an ideal system to experimentally test this basic principle probably underlying the evolution of sex.     

An epidemiological model of host–parasite coevolution and sex

The Red Queen hypothesis posits a promising way to explain the widespread existence of sexual reproduction despite the cost of producing males. The essence of the hypothesis is that coevolutionary interactions between hosts and parasites select for the genetic diversification of offspring via cross‐fertilization. Here, I relax a common assumption of many Red Queen models that each host is exposed to one parasite. Instead, I assume that the number of propagules encountered by each host depends on the number of infected hosts in the previous generation, which leads to additional complexities. The results suggest that epidemiological feedbacks, combined with frequency‐dependent selection, could lead to the long‐term persistence of sex under biologically reasonable conditions.     

Antagonistic Coevolution and Sex

One of the leading hypotheses for the maintenance of sexual reproduction is the Red Queen hypothesis. The underlying premise of the Red Queen hypothesis is that parasites rapidly evolve to infect common host genotypes. This response by parasites could result in the long-term maintenance of genetic variation and may favor sexual reproduction over asexual reproduction. The underlying ideas present a wonderful microcosm for teaching evolution. Here I present the reasons for why sex is anomalous for evolutionary theory, the rationale underlying the Red Queen hypothesis, and some empirical studies of the Red Queen hypothesis using a freshwater snail. The empirical results are consistent with the Red Queen hypothesis. In addition, the distribution of sexual and asexual reproduction in the snail leads naturally to thinking about coevolution in a geographic mosaic of parasite-mediated natural selection.     

The maintenance of sex: host–parasite coevolution with density‐dependent virulence

Why don’t asexual females replace sexual females in most natural populations of eukaryotes? One promising explanation is that parasites could counter the reproductive advantages of asexual reproduction by exerting frequency‐dependent selection against common clones (the Red Queen hypothesis). One apparent limitation of the Red Queen theory, however, is that parasites would seem to be required by theory to be highly virulent. In the present study, I present a population‐dynamic view of competition between sexual females and asexual females that interact with co‐evolving parasites. The results show that asexual populations have higher carrying capacities, and more unstable population dynamics, than sexual populations. The results also suggest that the spread of a clone into a sexual population could increase the effective parasite virulence as population density increases. This combination of parasite‐mediated frequency‐dependent selection, and density‐dependent virulence, could lead to the coexistence of sexual and asexual reproductive strategies and the long‐term persistence of sex.     

Sex differences in recombination

One of the stronger empirical generalizations to emerge from the study of genetic systems is that achiasmate meiosis, which has evolved 25–30 times, is always restricted to the heterogametic sex in dioecious species, usually the male. Here we collate data on quantitative sex differences in chiasma frequency from 54 species (4 hermaphroditic flatworms, 18 dioecious insects and vertebrates and 32 hermaphroditic plants) to test whether similar trends hold. Though significant sex differences have been observed within many species, only the Liliaceae show a significant sexual dimorphism in chiasma frequency across species, with more crossing over in embryo mother cells than in pollen mother cells; chiasma frequencies are unrelated to sex and gamety in all other higher taxa studied. Further, the magnitude of sexual dimorphism, independent of sign, does not differ among the three main ecological groups (dioecious animals, plants, and hermaphroditic animals), contrary to what would be expected if it reflected sex-specific selection on recombination. These results indicate that the strong trends for achiasmate meiosis do not apply to quantitative sex differences in recombination, and contradict theories of sex-specific costs and benefits. An alternative hypothesis suggests that sex differences may be more-or-less neutral, selection determining only the mean rate of recombination. While male and female chiasma frequencies are more similar than would be expected under complete neutrality, a less absolute form of the hypothesis is more difficult to falsify. In female mice the sex bivalent has more chiasmata for its length than the autosomes, perhaps compensating for the absence of recombination in males. Finally, we observe that chiasma frequencies in males and females are positively correlated across species, validating the use of only one sex in comparative studies of recombination.     

Sex versus parasitism versus density

The Red Queen hypothesis predicts that sexual reproduction should be favoured when the risk of infection by parasites is high. However, this prediction may also be achieved independently by means of the reproductive assurance and the density-dependent transmission hypotheses because higher densities increase the chances of fertilization (i.e. mates are easier to find) and increase the risk of infection. Additionally, the Red Queen hypothesis makes a long-term prediction that infection should be genotype-specific, with time-lagged dynamics. In the present study, we attempt to consolidate these two predictions by investigating whether sexuality and parasitism alternate in a time-lagged fashion on an ecological time-scale. In a 3-year study, we examined the time-lagged dynamics between male frequencies, infection levels (by Centrocestus sp.), and snail densities of four natural populations of sexual and asexual Melanoides tuberculata snails. The results obtained provide no evidence of either prediction of the Red Queen hypothesis. We found partial support for reproductive assurance in a single population, and could not discriminate between the three hypotheses in another population. The remaining two populations did not support any of the hypotheses in question.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 537–544.     

Parasite transmission among relatives halts Red Queen dynamics

The theory that coevolving hosts and parasites create a fluctuating selective environment for one another (i.e., produce Red Queen dynamics) has deep roots in evolutionary biology; yet empirical evidence for Red Queen dynamics remains scarce. Fluctuating coevolutionary dynamics underpin the Red Queen hypothesis for the evolution of sex, as well as hypotheses explaining the persistence of genetic variation under sexual selection, local parasite adaptation, the evolution of mutation rate, and the evolution of nonrandom mating. Coevolutionary models that exhibit Red Queen dynamics typically assume that hosts and parasites encounter one another randomly. However, if related individuals aggregate into family groups or are clustered spatially, related hosts will be more likely to encounter parasites transmitted by genetically similar individuals. Using a model that incorporates familial parasite transmission, we show that a slight degree of familial parasite transmission is sufficient to halt coevolutionary fluctuations. Our results predict that evidence for Red Queen dynamics, and its evolutionary consequences, are most likely to be found in biological systems in which hosts and parasites mix mainly at random, and are less likely to be found in systems with familial aggregation. This presents a challenge to the Red Queen hypothesis and other hypotheses that depend on coevolutionary cycling.     

Diversity and the maintenance of sex by parasites

The Red Queen hypothesis (RQH) predicts that parasite‐mediated selection will maintain sexual individuals in the face of competition from asexual lineages. The prediction is that sexual individuals will be difficult targets for coevolving parasites if they give rise to more genetically diverse offspring than asexual lineages. However, increasing host genetic diversity is known to suppress parasite spread, which could provide a short‐term advantage to clonal lineages and lead to the extinction of sex. We test these ideas using a stochastic individual‐based model. We find that if parasites are readily transmissible, then sex is most likely to be maintained when host diversity is high, in agreement with the RQH. If transmission rates are lower, however, we find that sexual populations are most likely to persist for intermediate levels of diversity. Our findings thus highlight the importance of genetic diversity and its impact on epidemiological dynamics for the maintenance of sex by parasites.     

Population structure, parasitism, and survivorship of sexual and autodiploid parthenogenetic Campeloma limum

Two theories for the maintenance of sexual reproduction, the Red Queen hypothesis and mutation accumulation, suggest that the dispersal rates of sexuals and asexuals may determine the elimination or persistence of asexuals. Under higher dispersal rates of asexuals, asexuals may temporarily escape virulent parasites and reduce the effects of deleterious mutations. In the present study, I examine the population structure, parasite loads, and juvenile survivorship of Campeloma limum sexuals and autodiploid parthenogens from the southeastern U.S. Atlantic coastal plain. Using mtDNA sequence variation, it is shown that parthenogenetic haplotypes with limited sequence divergence are geographically widespread throughout this region and there is no significant population differentiation over a broad geographical scale. Sexual C. limum populations show significant mtDNA differentiation among and within river drainages and there is significant isolation by distance. These patterns are consistent with a recent origin and range expansion of parthenogens. Prevalence of infection by digenetic trematodes is significantly higher in autodiploid parthenogens, and the variance of prevalence is also higher in autodiploid parthenogens. I argue that the latter pattern indicates that unparasitized parthenogens have temporarily escaped these virulent parasites, but recolonization of these populations by trematodes results in high infection levels (> 40%), possibly due to reduced variation in resistance genes. I also examined whether the survivorship of juvenile sexuals and parthenogens varied under different stress levels. Sexual juveniles had twofold higher survivorship in all environments. Compared to polyploid parthenogens, autodiploid parthenogens may be less buffered against the effects of deleterious recessive alleles. I propose that the combined effects of higher parasitism and reduced juvenile survivorship of these autodiploid parthenogens accounts for the spatial distribution of sexual and parthenogenetic C. limum in the Atlantic coastal plain. Parthenogens may persist by higher dispersal rates into marginal habitats where there is a temporary escape from digenetic trematodes and competition with sexuals.     

Production of germ line chimera by transfer of primordial germ cells in the domestic chicken (Gallus domesticus)

Blood was collected from Stage 13 to 14 (1) chick embryos. Primordial germ cells (PGCs) were separated from blood cells by Ficoll density gradient centrifugation. One hundred Rhode Island Red PGCs per embryo were transferred to the blood stream of Stage 14 to 15 White Leghorn embryos. Also, one hundred White Leghorn PGCs per embryo were transferred to the blood stream of Stage 14 to 15 Rhode Island Red embryos. Hatched male and female chicks were raised until sexual maturity, and progeny tests were performed by mating these PGC recipients with Rhode Island Red chickens of the opposite sex. Chicks apparently derived from the transferred PGCs, based on the feather color of the chicks, were produced from all 4 possible mating combinations. The present results indicate that the germ line of PGC recipient chickens consists of 2 distinct populations of germ cells.     

THE MAINTENANCE OF SEX BY PARASITISM AND MUTATION ACCUMULATION UNDER EPISTATIC FITNESS FUNCTIONS

The mutation accumulation hypothesis predicts that sex functions to reduce the population mutational load, while the Red Queen hypothesis holds that sex is adaptive as a defense against coevolving pathogens. We used computer simulations to examine the combined and separate effects of selection against deleterious mutations and host-parasite coevolution on the spread of a clone into an outcrossing sexual population. The results suggest that the two processes operating simultaneously may select for sex independent of the exact shape of the function that maps mutation number onto host fitness.     

Diverse,endemic and polyphyletic clones in mixed populations of a freshwater snail (Potamopyrgus antipodarum)

Understanding the source and diversity of clones is necessary to resolve the complicated issues surrounding the apparent evolutionary stability of sexual reproduction. The source of clones is important because present theory is based on an “all else equal” assumption, which is predicated on the idea that clonal mutants are derived from and compete with local sexual populations. Clonal diversity is important because it reduces the advantage of sexual reproduction under either soft selection (the Tangled Bank Hypothesis) or under strict frequency-dependent selection (the Red Queen Hypothesis). In the present study, protein electrophoresis was used to determine the source and diversity of clones in a freshwater snail (Potamopyrgus antipodarum) in four glacial lakes in which sexual and clonal females were thought to coexist. The results showed (1) that the populations were mixtures of diploid sexual and triploid asexual individuals, (2) that genotypic diversity of clonal populations is very high in all four lakes (but lower than in the sympatric sexual populations), and (3) that the clones are polyphyletically derived from their sympatric sexual populations. Consequently, repeated mutation to parthenogenetic reproduction since the Pleistocene has introduced a different and diverse set of clones in all four lakes. Such diversity may provide a challenge for the ecological theories of sex that rely on frequency-dependent selection.