Diets of sexual and sperm‐dependent asexual dace (Chrosomus spp.): relevance to niche differentiation and mate choice hypotheses for coexistence

Sperm‐dependent asexual species must coexist with a sexual species (i.e. a sperm source) to reproduce. The maintenance of this coexistence, and hence the persistence of sperm‐dependent asexual species, may depend on ecological niche separation or preference by males for conspecific (i.e. sexual) mates. We first modified an analytical model to consider both of these mechanisms acting simultaneously on the coexistence of the two species. Our model indicates that a small amount of niche separation between parental species and hybrids can facilitate coexistence by weakening the requirement for male mate preference. We also estimated niche separation empirically in the Chrosomus (formerly Phoxinus) sexual‐asexual system based on diet overlap between sperm‐dependent asexuals and their two sexual host species. Diet overlap between the sexual species was not significant in either lake, whereas the sperm‐dependent asexual had an intermediate niche that overlapped significantly, but somewhat asymmetrically, with both sexual species. These empirical results were then used to parameterize our analytical model to predict the minimum strength of male mate preference required to maintain coexistence in each lake. Some male mate preference is likely required to maintain coexistence in the Chrosomus system, but the minimum required preference depends on the severity of density dependence. Future empirical work on understanding coexistence in sperm‐dependent asexual systems would benefit from taking both niche separation and mate choice into account, and from simultaneous empirical estimates of male mate choice, niche separation, and density dependence.     

Evolution of cyclic sexual reproduction under host-parasite interactions

Alternate changes of sexual and asexual generations was studied theoretically by numerical analyses, from the viewpoint of host-parasite infective interactions. The host species was considered a diploid organism, characterized by two loci determining parasite resistance type and sexual strategy, between which a linkage exists to a certain degree. The sexual reproductive strategy was assumed to be determined by three alleles: asexual, complete sexual and cyclic sexual alleles. The effect of the parasites was represented by decreasing fitness functions of each host-type frequency. Numerical analyses of various linkages between genes and frequency dependence of host fitness revealed that the dynamics varied depending on whether the cyclic sexual allele was dominant or recessive against the complete sexual allele. When the cyclic sexual allele was dominant, the cyclic sexual strain persisted under intermediate frequency dependence of host fitness. On the other hand, when the cyclic sexual allele was recessive, it always tended to spread and to be maintained in the population. In such situations, both complete and cyclic sexual strains coexist, but the asexual strain is lost.     

How populations persist when asexuality requires sex: the spatial dynamics of coping with sperm parasites

The twofold cost of sex implies that sexual and asexual reproduction do not coexist easily. Asexual forms tend to outcompete sexuals but may eventually suffer higher extinction rates, creating tension between short- and long-term advantages of different reproductive modes. The 'short-sightedness' of asexual reproduction takes a particularly intriguing form in gynogenetic species complexes, in which an asexual species requires sperm from a related sexual host species to trigger embryogenesis. Asexuals are then predicted to outcompete their host, after which neither species can persist. We examine whether spatial structure can explain continued coexistence of the species complex, and assess the evidence based on data on the Amazon molly (Poecilia formosa). A modification of the Levins metapopulation model creates two regions of good prospects for coexistence, connected by a region of poorer patch occupancy levels. In the first case, mate discrimination and/or niche differentiation keep local extinction rates low, and most patches contain both species; the other possibility resembles host-parasite dynamics where parasites frequently drive the host locally extinct. Several dynamical features are counterintuitive and relate to the parasitic nature of interactions in the species complex: for example, high local extinction rates of the asexual species can be beneficial for its own persistence. This creates a link from the evolution of sexual reproduction to that of prudent predation.     

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.     

Density,parasitism, and sexual reproduction are strongly correlated in lake Daphnia populations

Many organisms can reproduce both asexually and sexually. For cyclical parthenogens, periods of asexual reproduction are punctuated by bouts of sexual reproduction, and the shift from asexual to sexual reproduction has large impacts on fitness and population dynamics. We studied populations of Daphnia dentifera to determine the amount of investment in sexual reproduction as well as the factors associated with variation in investment in sex. To do so, we tracked host density, infections by nine different parasites, and sexual reproduction in 15 lake populations of D. dentifera for 3 years. Sexual reproduction was seasonal, with male and ephippial female production beginning as early as late September and generally increasing through November. However, there was substantial variation in the prevalence of sexual individuals across populations, with some populations remaining entirely asexual throughout the study period and others shifting almost entirely to sexual females and males. We found strong relationships between density, prevalence of infection, parasite species richness, and sexual reproduction in these populations. However, strong collinearity between density, parasitism, and sexual reproduction means that further work will be required to disentangle the causal mechanisms underlying these relationships.     

How to go extinct by mating too much: population consequences of male mate choice and efficiency in a sexual–asexual species complex

Selection acting on individuals is not predicted to maximize population persistence, yet examples that explicitly quantify conflicts between individual and population level benefits are scarce. One such conflict occurs over sexual reproduction because of the cost of sex: sexual populations that suffer the cost of producing males have only half the growth rate compared to asexuals. Male behaviour can additionally impact population dynamics in a variety of ways, and here we study an example where the impact is unusually clear: the riddle of persistence of sperm‐dependent sexual–asexual species complexes. Here, a sexually reproducing host species coexists with an ameiotically reproducing all‐female sperm parasite. Sexual–asexual coexistence should not be stable because the proportion of asexually reproducing females will rapidly increase and the relative abundance of the sexually reproducing host species will decline. A severe shortage of males will lead to sperm limitation for sexual and asexual females and the system collapses. Male mate choice could reduce the reproductive potential of the asexual species and thus potentially prevent the collapse. In the gynogenetic (sperm‐dependent parthenogenetic) Amazon molly Poecilia formosa and its host (P. latipinna or P. mexicana), males discriminate against asexual females to some extent. Using a population‐dynamical model, we examine the population dynamics of this species complex with varying strengths of male discrimination ability and efficiency with which they locate females and produce sperm. The sexual species would benefit from stronger discrimination, thus preventing being displaced by the asexual females. However, males would be required to evolve preferences that are probably too strong to be purely based upon selection acting on individuals. We conclude that male behaviour does not fully prevent but delays extinction, yet this is highly relevant because low local extinction rates strongly promote coexistence as a metapopulation.     

The Ratchet and the Red Queen: the maintenance of sex in parasites

The adaptive significance of sexual reproduction remains as an unsolved problem in evolutionary biology. One promising hypothesis is that frequency‐dependent selection by parasites selects for sexual reproduction in hosts, but it is unclear whether such selection on hosts would feed back to select for sexual reproduction in parasites. Here we used individual‐based computer simulations to explore this possibility. Specifically, we tracked the dynamics of asexual parasites following their introduction into sexual parasite populations for different combinations of parasite virulence and transmission. Our results suggest that coevolutionary interactions with hosts would generally lead to a stable coexistence between sexual parasites and a single parasite clone. However, if multiple mutations to asexual reproduction were allowed, we found that the interaction led to the accumulation of clonal diversity in the asexual parasite population, which led to the eventual extinction of the sexual parasites. Thus, coevolution with sexual hosts may not be generally sufficient to select for sex in parasites. We then allowed for the stochastic accumulation of mutations in the finite parasite populations (Muller's Ratchet). We found that, for higher levels of parasite virulence and transmission, the population bottlenecks resulting from host–parasite coevolution led to the rapid accumulation of mutations in the clonal parasites and their elimination from the population. This result may explain the observation that sexual reproduction is more common in parasitic animals than in their free‐living relatives.     

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.     

Interactions between frequency-dependent and vertical transmission in host-parasite systems.

We investigate host-pathogen dynamics and conditions for coexistence in two models incorporating frequency-dependent horizontal transmission in conjunction with vertical transmission. The first model combines frequency-dependent and uniparental vertical transmission, while the second addresses parasites transmitted vertically via both parents. For the first model, we ask how the addition of vertical transmission changes the coexistence criteria for parasites transmitted by a frequency-dependent horizontal route, and show that vertical transmission significantly broadens the conditions for parasite invasion. Host-parasite coexistence is further affected by the form of density-dependent host regulation. Numerical analyses demonstrate that within a host population, a parasite strain with horizontal frequency-dependent transmission can be driven to extinction by a parasite strain that is additionally transmitted vertically for a wide range of parameters. Although models of asexual host populations predict that vertical transmission alone cannot maintain a parasite over time, analysis of our second model shows that vertical transmission via both male and female parents can maintain a parasite at a stable equilibrium. These results correspond with the frequent co-occurrence of vertical with sexual transmission in nature and suggest that these transmission modes can lead to host-pathogen coexistence for a wide range of systems involving hosts with high reproductive rates.     

Going solo: discovery of the first parthenogenetic gordiid (Nematomorpha: Gordiida)

Despite the severe fitness costs associated with sexual reproduction, its persistence and pervasiveness among multicellular organisms testifies to its intrinsic, short-term advantages. However, the reproductive assurance hypothesis predicts selection favoring asexual reproduction in sparse populations and when mate finding is difficult. Difficulties in finding mates is especially common in parasites, whose life cycles involve multiple hosts, or being released from the host into the external environment where the parasite can find itself trapped without a sexual partner. To solve this problem and guarantee reproduction, parasites in numerous phyla have evolved reproductive strategies, as predicted by the reproductive assurance hypothesis, such as hermaphroditism or parthenogenesis. However, this type of strategy has not been reported from species in the phylum Nematomorpha, whose populations have often been described as sparse. A new Nematomorpha species, Paragordius obamai n. sp., was discovered from Kenya, Africa, and appears to have solved the problem of being trapped without a mate by eliminating the need for males. Paragordius obamai n. sp. represents the first and only known species within this phylum to reproduce asexually. To determine the mechanism of this mating strategy, we ruled out the involvement of reproduction manipulating endosymbionts by use of next generation sequencing data, thus suggesting that parthenogenesis is determined genetically and may have evolved as a means to assure reproduction. Since this new parthenogenetic species and a closely related gonochoristic North American congener, P. varius, are easy to propagate in the laboratory, these gordiids can be used as model systems to test hypotheses on the genetic advantages and disadvantages of asexual reproduction and the genetic determinants of reproductive strategies in parasites.     

Polymorphic MHC loci in an asexual fish,the amazon molly (Poecilia formosa; Poeciliidae)

Genes of the major histocompatibility complex (MHC) encode molecules that control immune recognition and are highly polymorphic in most vertebrates. The remarkable polymorphisms at MHC loci may be maintained by selection from parasites, sexual selection, or both. If asexual species show equal (or higher) levels of polymorphisms at MHC loci as sexual ones, this would mean that sexual selection is not necessary to explain the high levels of diversity at MHC loci. In this study, we surveyed the MHC diversity of the asexual amazon molly (Poecilia formosa) and one of its sexual ancestors, the sailfin molly (P. latipinna), which lives in the same habitat. We found that the asexual molly has polymorphic MHC loci despite its clonal reproduction, yet not as polymorphic as the sexual species. Although the nucleotide diversity was similar between the asexual and sexual species, the sexual species exhibited a greater genotypic diversity compared to the asexual one from the same habitats. Within‐genome diversity was similar for MHC class I loci, but for class IIB, the sexual species had higher diversity compared to the asexual — despite the hybrid origins and higher levels of heterozygosity at microsatellite loci in the asexual species. The level of positive selection appears to be similar between the two species, which suggests that these polymorphisms are maintained by selection. Thus, our findings do not allow us to rule out the sexual selection hypothesis for the evolution of MHC diversity, and although the sexual fish has higher levels of MHC‐diversity compared to the asexual species, this may be due to differences in demography, parasites, or other factors, rather than sexual selection.     

Long-Distance Wind-Dispersal of Spores in a Fungal Plant Pathogen: Estimation of Anisotropic Dispersal Kernels from an Extensive Field Experiment

Given its biological significance, determining the dispersal kernel (i.e., the distribution of dispersal distances) of spore-producing pathogens is essential. Here, we report two field experiments designed to measure disease gradients caused by sexually- and asexually-produced spores of the wind-dispersed banana plant fungus Mycosphaerella fijiensis. Gradients were measured during a single generation and over 272 traps installed up to 1000 m along eight directions radiating from a traceable source of inoculum composed of fungicide-resistant strains. We adjusted several kernels differing in the shape of their tail and tested for two types of anisotropy. Contrasting dispersal kernels were observed between the two types of spores. For sexual spores (ascospores), we characterized both a steep gradient in the first few metres in all directions and rare long-distance dispersal (LDD) events up to 1000 m from the source in two directions. A heavy-tailed kernel best fitted the disease gradient. Although ascospores distributed evenly in all directions, average dispersal distance was greater in two different directions without obvious correlation with wind patterns. For asexual spores (conidia), few dispersal events occurred outside of the source plot. A gradient up to 12.5 m from the source was observed in one direction only. Accordingly, a thin-tailed kernel best fitted the disease gradient, and anisotropy in both density and distance was correlated with averaged daily wind gust. We discuss the validity of our results as well as their implications in terms of disease diffusion and management strategy.     

CORRELATED EVOLUTION OF SEXUAL SYSTEM AND LIFE-HISTORY TRAITS IN MOSSES

In mosses, separate and combined sexes are evolutionarily labile, yet factors selecting for this variation are unknown. In this study, we investigate phylogenetic correlations between sexual system and five life-history traits (asexual reproduction, chromosome number, gametophore length, spore size, and seta length). We assigned states to species on a large-scale phylogeny of mosses and used maximum likelihood analyses to test for the correlations and investigate the sequence of trait acquisition. Mosses in lineages with separate sexes were significantly more likely to be large, whereas those in lineages with combined sexes had higher chromosome numbers. Moreover, evolutionary transitions to separate sexes were more likely to occur in lineages with small spores. There was no support for a correlation between asexual reproduction and separate sexes. These results suggest that sexual system evolution is influenced by traits affecting mate availability and the dispersal of gametes and spores, and provides evidence for the existence of syndromes of life-history traits in mosses.     

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.     

A habitat colonisation model for spore-dispersed organisms—Does it work with eumycetozoans?

Spore productivities and establishment probabilities of eumycetozoans were estimated and compared with quantitative data obtained from field surveys, using series of cultures of a given substrate. Spore numbers per spore case were found to increase from one to four in protostelids to up to 10⁵–10⁶ in myxomycetes, whereas average spore size decreased slightly from 14.8 μm for protostelids to 10.3 μm in myxomycetes. Spore numbers of fructifications calculated from dimensions of spores and fruit bodies were in good agreement with direct counts carried out for six species of myxomycetes. A colonisation model is presented that estimates frequencies (as a percent of successfully colonized habitat islands), which is independent of a given density of spore rain and the sexual system of the species being considered. Whereas asexual species need a minimum spore rain of ca 0.7 spores per habitat island to reach a frequency of 50 %, this figure is at least 2.4-fold higher for sexual species, depending from the incompatibility system assumed. Data from cultures indicate that the maximum potential spore rain is usually three orders of magnitude higher than the minimum figure required to create the observed frequencies. Eumycetozoans seem to follow the evolutionary trends predicted by the model. Species with sexual reproductive systems produce often more spores than asexual ones; many morphospecies have sexual and asexual strains; and back-conversion from sexual to asexual reproduction occurs occasionally.     

Selection arena in Aspergillus nidulans

The selection arena hypothesis states that overproduction of zygotes--a widespread phenomenon in animals and plants--can be explained as a mechanism of progeny choice. As a similar mechanism, the ascomycetous fungus Aspergillus nidulans may overproduce dikaryotic fruit initials, hereafter called dikaryons. Then, progeny choice might involve selection on which of these dikaryons will thrive to produce thousands of zygotes. These zygotes each produce eight sexual spores which together fill up one fruiting body. In this study, we test the selection arena hypothesis in this homothallic fungus that produces both sexual and asexual spores. We analyzed two mitochondrial and 15 auxotrophic mutations for consequences on sexual and asexual reproduction. We found that many of these mutations confer sexual self-sterility as a pleiotropic effect under conditions of normal asexual spore production. This confirms an important prediction of the selection arena, namely that dikaryons carrying a (slightly) deleterious mutation are not able to proliferate and produce sexual spores. The selection arena ensures that reproductive energy is invested mainly in dikaryons and thus sexual spores of good genetic quality.     

Microsatellite and single‐nucleotide polymorphisms indicate recurrent transitions to asexuality in a microsporidian parasite

Assessing the mode of reproduction of microparasites remains a difficult task because direct evidence for sexual processes is often absent and the biological covariates of sex and asex are poorly known. Species with geographically divergent modes of reproduction offer the possibility to explore some of these covariates, for example, the influence of life‐history traits, mode of transmission and life‐cycle complexity. Here, we present a phylogeographical study of a microsporidian parasite, which allows us to relate population genetic structure and mode of reproduction to its geographically diverged life histories. We show that in microsporidians from the genus Hamiltosporidium, that use the cladoceran Daphnia as host, an epidemic population structure has evolved, most probably since the last Ice Age. We partially sequenced three housekeeping genes (alpha tubulin, beta tubulin and hsp70) and genotyped seven microsatellite loci in 51 Hamiltosporidium isolates sampled within Europe and the Middle East. We found two phylogenetically related asexual parasite lines, one each from Fennoscandia and Israel, which share the unique ability of being transmitted both vertically and horizontally from Daphnia to Daphnia. The sexual forms cannot transmit horizontally among Daphnia, but presumably have a complex life cycle with a second host species. In spite of the similarities between the two asexual lineages, a clustering analysis based on microsatellite polymorphisms shows that asexual Fennoscandian parasites do not share ancestry with any other Hamiltosporidium that we have sampled. Moreover, allele sequence divergence at the hsp70 locus is twice as large in Fennoscandian than in Israeli parasites. Our results indicate that asexual reproduction evolved twice independently, first in Fennoscandian and more recently in the Israeli parasites. We conclude that the independent origin of asexuality in these two populations is associated with the altered parasite mode of transmission and the underlying dynamics of host populations.     

Prezygotic isolation between Saccharomyces cerevisiae and Saccharomyces paradoxus through differences in mating speed and germination timing

Although prezygotic isolation between sympatric populations of closely related animal and plant species is well documented, far less is known about such evolutionary phenomena in sexual microbial species, as most are difficult to culture and manipulate. Using the molecular and genetic tools available for the unicellular fungus Saccharomyces cerevisiae, and applying them to S. paradoxus, we tested the behavior of individual cells from sympatric woodland populations of both species for evidence of prezygotic isolation. First, we confirmed previous observations that vegetative cells of both species mate preferentially with S. cerevisiae. Next, we found evidence for mate discrimination in spores, the stage in which outcrossing opportunities are most likely to occur. There were significant differences in germination timing between the species: under the same conditions, S. paradoxus spores do not begin germinating until almost all S. cerevisiae spores have finished. When germination time was staggered, neither species discriminated against the other, suggesting that germination timing is responsible for the observed mate discrimination. Our results indicate that the mechanisms of allochronic isolation that are well known in plants and animals can also operate in sexual microbes.     

Host-parasite population dynamics under combined frequency- and density-dependent transmission

Many host‐parasite models assume that transmission increases linearly with host population density (‘density‐dependent transmission’), but various alternative transmission functions have been proposed in an effort to capture the complexity of real biological systems. The most common alternative (usually applied to sexually transmitted parasites) assumes instead that the rate at which hosts contact one another is independent of population density, leading to ‘frequency‐dependent’ transmission. This straight‐forward distinction generates fundamentally different dynamics (e.g. deterministic, parasite‐driven extinction with frequency‐ but not density‐dependence). Here, we consider the situation where transmission occurs through two different types of contact, one of which is density‐dependent (e.g. social contacts), the other density‐independent (e.g. sexual contacts). Drawing on a range of biological examples, we propose that this type of contact structure may be widespread in natural populations. When our model is characterized mainly by density‐dependent transmission, we find that allowing even small amounts of transmission to occur through density‐independent contacts leads to the possibility of deterministic, parasite‐driven extinction (and lowers the threshold for parasite persistence). Contrastingly, allowing some density‐dependent transmission to occur in a model characterized mainly by density‐independent contacts (i.e. by frequency‐dependent transmission) does not affect the extinction threshold, but does increase the likelihood of parasite persistence. The idea that directly transmitted parasites exploit different types of host contact is not new, but here we show that the impact on dynamics can be fundamental even in the simplest cases. For example, in systems where density‐dependent transmission is normally assumed de facto, we show that parasite‐driven extinction can occur if a small amount of transmission occurs through density‐independent contacts. Many empirical studies are still guided by the traditional density/frequency dichotomy, but our combined transmission function may provide a better model for systems in which both types of transmission occur.     

The maintenance of sex in parasites

The maintenance of sex is an unresolved paradox in evolutionary biology, given the inherent twofold fitness advantage for asexuals. Parasitic helminths offer a unique opportunity to address this enigma. Parasites that can create novel antigenic strains are able to escape pre-existing host immunity. Viruses produce diversity through mutation with rapid clonal proliferation. The long generation times of helminth parasites prevent them from adopting this strategy. Instead, we argue that sexual reproduction enables parasitic helminths to rapidly generate strain diversity. We use both a stochastic, individual-based model and a simple analytical model to assess the selective value of sexual versus asexual reproduction in helminth parasites. We demonstrate that sexual reproduction can more easily produce and maintain strain diversity than asexual reproduction for long-lived parasites. We also show that sexual parasite populations are resistant to invasion by rare asexual mutants. These results are robust to high levels of cross-immunity between strains. We suggest that the enhancement of strain diversity, despite stochastic extinction of strains, may be critical to the evolutionary success of sex in long-lived parasites.