Sexual Lineages Research Articles

EVOLUTION OF ASEXUALITY VIA DIFFERENT MECHANISMS IN GRASS THRIPS (THYSANOPTERA:Aptinothrips)

Asexual lineages can derive from sexual ancestors via different mechanisms and at variable rates, which affects the diversity of the asexual population and thereby its ecological success. We investigated the variation and evolution of reproductive systems in Aptinothrips, a genus of grass thrips comprising four species. Extensive population surveys and breeding experiments indicated sexual reproduction in A. elegans, asexuality in A. stylifer and A. karnyi, and both sexual and asexual lineages in A. rufus. Asexuality in A. stylifer and A. rufus coincides with a worldwide distribution, with sexual A. rufus lineages confined to a limited area. Inference of molecular phylogenies and antibiotic treatment revealed different causes of asexuality in different species. Asexuality in A. stylifer and A. karnyi has most likely genetic causes, while it is induced by endosymbionts in A. rufus. Endosymbiont-community characterization revealed presence of Wolbachia, and lack of other bacteria known to manipulate host reproduction. However, only 69% asexual A. rufus females are Wolbachia-infected, indicating that either an undescribed endosymbiont causes asexuality in this species or that Wolbachia was lost in several lineages that remained asexual. These results open new perspectives for studies on the maintenance of mixed sexual and asexual reproduction in natural populations.

Why is sex so rare in Lecane inermis (Rotifera: Monogononta) in wastewater treatment plants?

AbstractThe monogonont rotifer Lecane inermis is commonly known as a facultative parthenogen. Unexpectedly, among numerous lineages we isolated from wastewater treatment plants (WWTP), only one was capable of sexual reproduction. We investigated why sex was so rare among L. inermis in WWTP. The reproductive modes of lineages derived from the sexual lineage were examined. Among all lineages, the fraction of those reproducing only asexually for 14 d was 0.39. In the subsequent round, the fraction of asexual lineages reached 0.61. The population growth rate of the parthenogenetic lineages was significantly higher than that of the sexual lineages. We simulated the fate of rotifer populations in WWTP by removing 10% of the experimental cultures each day. After 10 d of these conditions, the mean number of females was greater in parthenogenetic than in sexual lineages. After 20 d, only solitary dormant eggs remained in the sexual lineages. It therefore appears that the loss of sex may be attributed to the specific conditions of the WWTP. When there is no risk of desiccation and no need for dormancy, the fast‐growing parthenogens outcompete lineages investing in costly sex. Furthermore, even if some resting eggs were deposited, they would be washed out from the system with the excess sludge.

Mating systems and selection efficacy: a test using chloroplastic sequence data in Angiosperms

Selfing is assumed to reduce selection efficacy, especially purifying selection. This can be tested using molecular data, for example by comparing the Dn/Ds ratio between selfing and outcrossing lineages. So far, little evidence of relaxed selection against weakly deleterious mutations (as inferred by a higher Dn/Ds ratio) in selfers as compared to outcrossers has been found, contrary to the pattern often observed between asexual and sexual lineages. However, few groups have been studied to date. To further test this hypothesis, we compiled and analysed chloroplastic sequence data sets in several plant groups. We found a general trend towards relaxed selection in selfers in our data sets but with weak statistical support. Simulations suggested that the results were compatible with weak-to-moderate Dn/Ds ratio differences in selfing lineages. Simple theoretical predictions also showed that the ability to detect relaxed selection in selfers could strongly depend on the distribution of the effects of deleterious mutations on fitness. Our results are compatible with a recent origin of selfing lineages whereby deleterious mutations potentially have a strong impact on population extinction or with a more ancient origin but without a marked effect of deleterious mutations on the extinction dynamics.

Allee Effects and the Evolution of Polymorphism in Cyclic Parthenogens

Cyclic parthenogens alternate asexual reproduction with periodic episodes of sexual reproduction. Sexually produced free-living forms are often their only way to survive unfavorable periods. When sexual reproduction requires the mating of two self-incompatible individuals, mating limitation may generate an Allee effect, which makes small populations particularly vulnerable to extinction; parthenogenetic reproduction can attenuate this effect. However, asexual reproduction likely trades off with sexual reproduction. To explore the evolutionary implications of such a trade-off, we included recurrent mating events associated with seasonal interruptions in a simple population dynamics model. Following an adaptive dynamics approach, we showed that positive density dependence associated with Allee effects in cyclic parthenogens promotes evolutionary divergence in the level of investment in asexual reproduction. Although polymorphism may be transient, morphs mostly investing into sexual reproduction may eventually exclude those predominantly reproducing in an asexual manner. Asexual morphs can be seen as making cooperative investments into the common pool of mates, while sexual morphs defect, survive better, and may eventually fix in the population. Our findings provide a novel hypothesis for the frequent coexistence of sexual and asexual lineages, notably in plant parasitic fungi.

Origin and Genetic Diversity of Diploid Parthenogenetic Artemia in Eurasia

There is wide interest in understanding how genetic diversity is generated and maintained in parthenogenetic lineages, as it will help clarify the debate of the evolution and maintenance of sexual reproduction. There are three mechanisms that can be responsible for the generation of genetic diversity of parthenogenetic lineages: contagious parthenogenesis, repeated hybridization and microorganism infections (e.g. Wolbachia). Brine shrimps of the genus Artemia (Crustacea, Branchiopoda, Anostraca) are a good model system to investigate evolutionary transitions between reproductive systems as they include sexual species and lineages of obligate parthenogenetic populations of different ploidy level, which often co-occur. Diploid parthenogenetic lineages produce occasional fully functional rare males, interspecific hybridization is known to occur, but the mechanisms of origin of asexual lineages are not completely understood. Here we sequenced and analysed fragments of one mitochondrial and two nuclear genes from an extensive set of populations of diploid parthenogenetic Artemia and sexual species from Central and East Asia to investigate the evolutionary origin of diploid parthenogenetic Artemia, and geographic origin of the parental taxa. Our results indicate that there are at least two, possibly three independent and recent maternal origins of parthenogenetic lineages, related to A. urmiana and Artemia sp. from Kazakhstan, but that the nuclear genes are very closely related in all the sexual species and parthenogegetic lineages except for A. sinica, who presumable took no part on the origin of diploid parthenogenetic strains. Our data cannot rule out either hybridization between any of the very closely related Asiatic sexual species or rare events of contagious parthenogenesis via rare males as the contributing mechanisms to the generation of genetic diversity in diploid parthenogenetic Artemia lineages.

Coexistence of sexual individuals and genetically isolated asexual counterparts in a thrips

Sex is a paradoxical phenomenon because it is less efficient compared with asexual reproduction. To resolve this paradox we need a direct comparison between sexual and asexual forms. In many organisms, however, sexual and asexual forms do not occur in the same habitat, or at the same time. In a few cases where sexual and asexual forms are found in a single population, some (though rare) genetic exchange is usually detected between the two forms. When genetic exchange occurs a direct comparison is impossible. Here we investigate a thrips exhibiting both sexual and asexual forms (lineages) that are morphologically indistinguishable. We examine if the two forms are genetically isolated. Phylogeny based on nuclear genes confirms that the sexual and asexual lineages are genetically differentiated. Thus we demonstrate that the current system has certain advantages over existing and previously used model systems in the evolution of sexual reproduction.

LET US NOT BE UNFAIR TO ASEXUALS: THEIR EPHEMERALITY MAY BE EXPLAINED BY NEUTRAL MODELS WITHOUT INVOKING ANY EVOLUTIONARY CONSTRAINTS OF ASEXUALITY

Phylogenetic studies typically demonstrate lower evolutionary ages of clones, relative to their sexual ancestors. This has often been attributed to heightened extinction risk of asexual organisms. We previously criticized such interpretations and demonstrated that the life span of clones is ultimately limited by neutral drift depending on the rate at which new clones are spawned into an asexual community of a finite size. Therefore, it is important to investigate whether the natural rates of such influxes are sufficiently high to account for the relative ephemerality of clones without assuming their increased extinction rate. I applied the neutral clonal turnover model to phylogenies of polyploid asexual ferns and simulated the coalescent trees over a wide range of demographic structures and sampling schemes. On parameterizing the model with biologically relevant estimates of population sizes and plant polyploidization rates, simulated clonal assemblages appeared younger than their sexual counterparts even in the absence of selection against clones. Therefore, differences observed between the ages of sexual and clonal lineages may be explained by the neutral clonal turnover. Researchers should consider the possibility that natural clones may get lost by neutral drift before their fate could eventually be affected by any long-term constraints of asexuality.

Clonal diversity driven by parasitism in a freshwater snail

One explanation for the widespread abundance of sexual reproduction is the advantage that genetically diverse sexual lineages have under strong pressure from virulent coevolving parasites. Such parasites are believed to track common asexual host genotypes, resulting in negative frequency-dependent selection that counterbalances the population growth-rate advantage of asexuals in comparison with sexuals. In the face of genetically diverse asexual lineages, this advantage of sexual reproduction might be eroded, and instead sexual populations would be replaced by diverse assemblages of clonal lineages. We investigated whether parasite-mediated selection promotes clonal diversity in 22 natural populations of the freshwater snail Melanoides tuberculata. We found that infection prevalence explains the observed variation in the clonal diversity of M.tuberculata populations, whereas no such relationship was found between infection prevalence and male frequency. Clonal diversity and male frequency were independent of snail population density. Incorporating ecological factors such as presence/absence of fish, habitat geography and habitat type did not improve the predictive power of regression models. Approximately 11% of the clonal snail genotypes were shared among 2-4 populations, creating a web of 17 interconnected populations. Taken together, our study suggests that parasite-mediated selection coupled with host dispersal ecology promotes clonal diversity. This, in return, may erode the advantage of sexual reproduction in M.tuberculata populations.

The distribution of sexual reproduction of the geographic parthenogenEucypris virens(Crustacea: Ostracoda) matches environmental gradients in a temporary lake

Niche segregation may prevent competitive exclusion and promote local coexistence. This typically results in the occupation of different habitats. In the freshwater ostracod Eucypris virens (Jurine, 1820), the distribution of sexual and parthenogenetic populations in the temporary Lake Caracuel, central Spain, was not homogeneous. Parthenogens were found everywhere including the littoral, whereas sexuals were restricted to the centre. We investigated the hypothesis that spatial distribution responded to ecological differences. We studied the ecological significance of this segregation by linking environmental data to male presence, sexual fraction, ploidy, and genetic structure of our model organism in 12 ponds in the lake basin. Hydro-chemical and biological data indicated that the observed segregation is not only spatial but also ecological, with sexual E. virens occurring in ponds with shorter and probably more unpredictable hydroperiod. The correlations between environmental gradients and E. virens population structure suggest that sexual and parthenogenetic lineages are ecologically segregated. Sexual populations appeared restricted to sufficiently unpredictable environments, while parthenogens dominated environments with longer hydroperiods. Local coexistence seems mediated by spatial heterogeneity in habitat stability.

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.

Linking present environment and the segregation of reproductive modes (geographical parthenogenesis) in Eucypris virens (Crustacea: Ostracoda)

AbstractAimGeographical parthenogenesis – in which parthenogenetic populations are more widely distributed than sexually reproducing populations – is observed in many plant and animal species. Many hypotheses have been proposed to account for this biogeographical pattern, and these often invoke historical processes such as the influence of glaciation. However, there are relatively few empirical studies of the contemporary factors associated with geographical parthenogenesis. The aim of this study was to understand its causes by linking contemporary environmental gradients with reproductive modes in the freshwater ostracod Eucypris virens.LocationEurope and North Africa.MethodsWe sampled populations of E. virens from 147 sites in 20 countries from Estonia to Morocco and from Portugal to Turkey. At each site we measured aspects of pond geography (latitude, longitude, elevation, pond area and depth), water chemistry (temperature, pH, conductivity, oxygen and ion concentrations) and macroinvertebrate assemblages. We used principal components and logistic regression analyses to test for the associations between environmental variables and the presence of males, indicating sexual reproduction, in a population.ResultsSexual populations were restricted to the Mediterranean, whereas parthenogenetic populations extended into the Baltic and Ponto‐Caspian areas. Significant environmental features were not only latitude, but also elevation, aridity and principal components summarizing water chemistry and invertebrate communities: sexual populations were more common at high elevations, in arid regions, and in turbid ponds. Ponds harbouring exclusively parthenogenetic populations were also characterized by having longer‐hydroperiod biological communities.Main conclusionsThe link between current environmental conditions and the reproductive modes of E. virens suggests a contemporary adaptation besides historical factors such as climatic cycles or the differential colonization success of sexual and asexual lineages. We propose that the pattern of geographical parthenogenesis in E. virens reflects the ability of asexual populations to colonize rapidly, and the higher adaptability of sexual populations to unpredictable hydroperiods.

Functional rare males in diploid parthenogeneticArtemia

Functional males that are produced occasionally in some asexual taxa - called 'rare males' - raise considerable evolutionary interest, as they might be involved in the origin of new parthenogenetic lineages. Diploid parthenogenetic Artemia produce rare males, which may retain the ability to mate with females of related sexual lineages. Here, we (i) describe the frequency of male progeny in populations of diploid parthenogenetic Artemia, (ii) characterize rare males morphologically, (iii) assess their reproductive role, using cross-mating experiments with sexual females of related species from Central Asia and characterize the F1 hybrid offspring viability and (iv) confirm genetically both the identity and functionality of rare males using DNA barcoding and microsatellite loci. Our result suggests that these males may have an evolutionary role through genetic exchange with related sexual species and that diploid parthenogenetic Artemia is a good model system to investigate the evolutionary transitions between sexual species and parthenogenetic strains.

Spermatozoa Production by Triploid Males in the New Zealand Freshwater Snail Potamopyrgus antipodarum.

Asexual lineages derived from dioecious taxa are typically assumed to be all female. Even so, asexual females from a variety of animal taxa occasionally produce males. The existence of these males sets the stage for potential gene flow across asexual lineages as well as between sexual and asexual lineages. A recent study showed that asexual triploid female Potamopyrgus antipodarum, a New Zealand freshwater snail often used as a model to study sexual reproduction, occasionally produce triploid male offspring. Here, we show that these triploid male P. antipodarum (1) have testes that produce morphologically normal sperm, (2) make larger sperm cells that contain more nuclear DNA than the sperm produced by diploid sexual males, and (3) produce sperm that range in DNA content from haploid to diploid, and are often aneuploid. Analysis of meiotic chromosomes of triploid males showed that aberrant pairing during prophase I probably accounts for the high variation in DNA content among sperm. These results indicate that triploid male P. antipodarum produce sperm, but the extent to which these sperm are able to fertilize female ova remains unclear. Our results also suggest that the general assumption of sterility in triploid males should be more closely examined in other species in which such males are occasionally produced. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110, 227–234.

Reproductive effort of Mastocarpus papillatus (Rhodophyta) along the California coast.

Species with sexual and asexual life cycles may exhibit intraspecific differences in reproductive effort. The spatial separation of sexual and asexual lineages, called geographic parthenogenesis, is common in plants, animals and algae. Mastocarpus papillatus is a well-documented case of geographic parthenogenesis in which sexuals dominate southern populations, asexuals dominate northern populations, while mixed populations occur throughout central California. We quantified abundances and reproductive effort of sexual and asexual fronds and tetrasporophytes at eight sites in California to test the hypotheses that (1) reduced sexual reproduction at higher latitudes and tidal heights explains the observed geographic parthenogenesis and (2) reproductive effort (spore production per blade area) declines with increasing latitude. Abundances of all phases varied site-specifically. However, there was no geographic pattern of reproductive effort of fronds. Reproductive effort of fronds was greater in 2006 than in 2007 and correlated with sea surface temperatures. Sexual fronds exhibited greater reproductive effort than did asexual fronds and sexual reproductive effort was also inversely correlated with local upwelling index. Tetrasporophytes showed greater reproductive effort in northern sites, but total supply of tetraspores per m2 was greatest in the middle of the sampling range where crusts were more abundant. There was no decline of reproductive effort at higher latitudes. Geographic patterns of fecundity of life stages do not explain geographic parthenogenesis in M. papillatus. Site-specific differences in viability among spores or established thalli of different life cycles may explain their respective geographic distributions, as the sexual and asexual life cycles responded differently to environmental variations.

Sexually Antagonistic Coevolution for Sexual Harassment Can Act as a Barrier to Further Invasions by Parthenogenesis

The assumption of a twofold cost of sex not only complicates the maintenance of sex but also sets conditions for sexual conflict: in organisms with the twofold cost, males often sexually harass females. Sexual harassment is detrimental to female fitness and thus might help maintain sexual populations if male harassment inflicts a harsher cost on parthenogens than on sexual females (asymmetric harassment cost). However, the generality of this concept is now considered doubtful because selective harassment of parthenogens results in loss of mating opportunities for males. Using three mathematical models, I show here that sexual harassment still can impose the asymmetric cost on parthenogens. First, I apply the Lotka-Volterra model to show the degree of asymmetric harassment cost that permits sex to be maintained stably in the population. Second, using adaptive dynamics, I examine whether sexually antagonistic coevolution for sexual harassment, which occurs only in sexual populations, can promote the asymmetric harassment cost. Finally, an individual-based model, which assumes a spatial structure unlike that in the other two, demonstrates that the asymmetric evolution of harassment cost prevents further invasions of parthenogens from different patches into sexual lineages; these mechanisms may account for allopatric distributions of sexual and parthenogenetic lineages as well as the maintenance of sex.

Characterization of transcriptomes from sexual and asexual lineages of a New Zealand snail (Potamopyrgus antipodarum)

Understanding the evolution and maintenance of sexual reproduction is one of the central challenges of evolutionary biology, yet we know very little about how sex influences molecular evolution. The New Zealand freshwater snail Potamopyrgus antipodarum is ideally suited to address this knowledge gap because obligately sexual individuals often coexist with multiple independently derived obligately asexual lineages. This unusual situation allows direct comparisons both between sexual and asexual P. antipodarum and across populations that differ in the relative frequency of sexual individuals. As such, P. antipodarum has received a great deal of attention as a model system for the maintenance of sex in nature and is also used as a model for environmental toxicology and biological invasions. Molecular genetic resources for P. antipodarum will thus be useful to investigators in a variety of biological fields. We used 454 sequencing of cDNA libraries to generate transcriptomes from two sexual and two asexual P. antipodarum lineages. A de novo assembly of 116.7Mb of sequence reads produced 41396 contigs, and sequence similarity-based Gene Ontology annotations were obtained for 3740 contigs. We detected 408315 SNP loci and 7315 microsatellite loci, which together represent the first genome-scale resource available for P. antipodarum. Raw 454 read sequences, contig sequences, annotation data and polymorphism data are publicly available in a searchable online database and for download at http://www.biology.uiowa.edu/neiman/transcriptome.php.

Low parasitism rates in parthenogenetic bagworm moths do not support the parasitoid hypothesis for sex

The parasite hypothesis for sex is one of the many theories that have been suggested to solve the mystery of the widespread occurrence of sex despite its high short-term costs. It suggests that sexual lineages have an evolutionary advantage over parthenogens because they can frequently generate new genotypes that are temporarily less prone to coevolving parasites. In this study, we looked for further supporting evidence for the parasite hypothesis of sex in an attempt to understand the coexistence of sexual and parthenogenetic bagworm moths (Naryciinae). The bagworm moths and their parasitoids form one of the few natural host-parasite systems where sexual and parthenogenetic hosts are apparently not separated by ecological or geographical barriers. Furthermore, in support of the parasite hypothesis for sex, parthenogenetic presence is negatively correlated with parasitism rate. We specifically tested, by identifying the reproductive mode of the parasitized individuals, whether parasitoids preferentially attack the parthenogens in sites with both sexual and parthenogenetic forms, as predicted by the parasite hypothesis. We collected hosts from sites with different frequencies of parthenogenetic and sexual moths. A DNA barcoding approach was used to determine the reproductive mode of the parasitized hosts. Furthermore, we investigated whether differences in host and parasitoid phenology could provide an alternative explanation for the variation in parasitism rates between parthenogens and sexuals. Our results contradict the prediction of the parasite hypothesis because parthenogenetic bagworm moths were less parasitized than sexuals in sympatric sites. Our findings can be explained by differences in phenology between the parthenogenetic and sexual moths rather than genetic incompatibility between parthenogenetic hosts and parasitoids. The stable coexistence of sexual and parthenogenetic Naryciinae despite the many apparent costs of sex in this system remains a mystery. Our work adds to the list of studies were the assumptions of the parasite hypothesis for sex are not all met.

Transposable element proliferation as a possible side effect of endosymbiont manipulations

The mode of reproduction has been predicted to affect the proliferation of transposable elements (TEs). A population that switches from sexual to asexual reproduction could either accumulate TEs because purifying selection becomes less efficient, or a decrease in TE load because the opportunity for horizontal transmission is reduced. A third possibility is that the mechanism that induces asexual reproduction affects TE dynamics as a side effect. We propose two such mechanisms that might explain recently described patterns of TE abundance in sexual and asexual lineages of the parasitoid wasp Leptopilina clavipes. Asexual reproduction in this species is induced by endosymbiotic Wolbachia bacteria. In order to achieve parthenogenesis in its host, Wolbachia might remove methylation or interfere with Argonaute proteins. Both methylation and Argonaute proteins are known to control TE activity in other species. By interfering with either, Wolbachia might therefore secondarily hamper the control of specific TEs.

Asexual evolution: do intragenomic parasites maintain sex?

Resolving the paradox of sex, with its twofold cost to genic transmission, remains one of the major unresolved questions in evolutionary biology. Counting this genetic cost has now gone genomic. In this issue of Molecular Ecology, Kraaijeveld et al. (2012) describe the first genome-scale comparative study of related sexual and asexual animal lineages, to test the hypothesis that asexuals bear heavier loads of deleterious transposable elements. A much higher density of such parasites might be expected, due to the inability of asexual lineages to purge transposons via mechanisms exclusive to sexual reproduction. They find that the answer is yes--and no--depending upon the family of transposons considered. Like many such advances in testing theory, more questions are raised by this study than answered, but a door has been opened to molecular evolutionary analyses of how responses to selection from intragenomic parasites might mediate the costs of sex.

Modelling the geographical range of a species with variable life-history.

We show how a climatic niche model can be used to describe the potential geographic distribution of a pest species with variable life-history, and illustrate how to estimate biogeographic pest threats that vary across space. The models were used to explore factors that affect pest risk (irrigation and presences of host plant). A combination of current distribution records and published experimental data were used to construct separate models for the asexual and sexual lineages of Rhopalosiphum padi (Linnaeus) (Hemiptera: Aphididae). The two models were combined with knowledge of host plant presence to classify the global pest risk posed by R. padi. Whilst R. padi has a relatively limited area in which sexual lineages can persist year round, a much larger area is suitable for transient sexual and asexual lineages to exist. The greatest risk of establishment of persistent sexual and asexual populations is in areas with warm temperate climates. At the global scale the models show very little difference in risk patterns between natural rainfall and irrigation scenarios, but in Australia, the amount of land suitable for persistent asexual and transient sexual populations decreases (by 20%) if drought stress is no longer alleviated by irrigation. This approach proved useful for modelling the potential distribution of a species that has a variable life-history. We were able to use the model outputs to examine factors such as irrigation practices and host plant presence that altered the nature (transient or permanent) and extent of pest risk. The composite niche maps indicate pest risk in terms that are useful to both biosecurity agencies and pest managers.