Asexual Experimental Evolution of Yeast Does Not Curtail Transposable Elements

Compared with asexual reproduction, sex facilitates the transmission of transposable elements (TEs) from one genome to another, but boosts the efficacy of selection against deleterious TEs. Thus, theoretically, it is unclear whether sex has a positive net effect on TE’s proliferation. An empirical study concluded that sex is at the root of TE’s evolutionary success because the yeast TE load was found to decrease rapidly in approximately 1,000 generations of asexual but not sexual experimental evolution. However, this finding contradicts the maintenance of TEs in natural yeast populations where sexual reproduction occurs extremely infrequently. Here, we show that the purported TE load reduction during asexual experimental evolution is likely an artifact of low genomic sequencing coverages. We observe stable TE loads in both sexual and asexual experimental evolution from multiple yeast data sets with sufficient coverages. To understand the evolutionary dynamics of yeast TEs, we turn to asexual mutation accumulation lines that have been under virtually no selection. We find that both TE transposition and excision rates per generation, but not their difference, tend to be higher in environments where yeast grows more slowly. However, the transposition rate is not significantly higher than the excision rate and the variance of the TE number among natural strains is close to its neutral expectation, suggesting that selection against TEs is at best weak in yeast. We conclude that the yeast TE load is maintained largely by a transposition–excision balance and that the influence of sex remains unclear.     

Sex drives intracellular conflict in yeast

Theory predicts that sex can drive the evolution of conflict within the cell. During asexual reproduction, genetic material within the cell is inherited as a single unit, selecting for cooperation both within the genome as well as between the extra‐genomic elements within the cell (e.g. plasmids and endosymbionts). Under sexual reproduction, this unity is broken down as parental genomes are distributed between meiotic progeny. Genetic elements able to transmit to more than 50% of meiotic progeny have a transmission advantage over the rest of the genome and are able to spread, even where they reduce the fitness of the individual as a whole. Sexual reproduction is therefore expected to drive the evolution of selfish genetic elements (SGEs). Here, we directly test this hypothesis by studying the evolution of two independent SGEs, the 2‐μm plasmid and selfish mitochondria, in populations of Saccharomyces cerevisiae. Following 22 rounds of sexual reproduction, 2‐μm copy number increased by approximately 13.2 (± 5.6) copies per cell, whereas in asexual populations copy number decreased by approximately 5.1 (± 1.5) copies per cell. Given that the burden imposed by this parasite increases with copy number, these results support the idea that sex drives the evolution of increased SGE virulence. Moreover, we found that mitochondria that are respiratory‐deficient rapidly invaded sexual but not asexual populations, demonstrating that frequent outcrossed sex can drive the de novo evolution of genetic parasites. Our study highlights the genomic perils of sex and suggests that SGEs may play a key role in driving major evolutionary transitions, such as uniparental inheritance.     

Genetic variation and asexual reproduction in the facultatively parthenogenetic cockroach Nauphoeta cinerea: implications for the evolution of sex

Asexual reproduction could offer up to a two‐fold fitness advantage over sexual reproduction, yet higher organisms usually reproduce sexually. Even in facultatively parthenogenetic species, where both sexual and asexual reproduction is sometimes possible, asexual reproduction is rare. Thus, the debate over the evolution of sex has focused on ecological and mutation‐elimination advantages of sex. An alternative explanation for the predominance of sex is that it is difficult for an organism to accomplish asexual reproduction once sexual reproduction has evolved. Difficulty in returning to asexuality could reflect developmental or genetic constraints. Here, we investigate the role of genetic factors in limiting asexual reproduction in Nauphoeta cinerea, an African cockroach with facultative parthenogenesis that nearly always reproduces sexually. We show that when N. cinerea females do reproduce asexually, offspring are genetically identical to their mothers. However, asexual reproduction is limited to a nonrandom subset of the genotypes in the population. Only females that have a high level of heterozygosity are capable of parthenogenetic reproduction and there is a strong familial influence on the ability to reproduce parthenogenetically. Although the mechanism by which genetic variation facilitates asexual reproduction is unknown, we suggest that heterosis may facilitate the switch from producing haploid meiotic eggs to diploid, essentially mitotic, eggs.     

Biological species is the only possible form of existence for higher organisms: the evolutionary meaning of sexual reproduction

   

Consistent holistic view of sexual species as the highest form of biological existence is presented. The Weismann's idea that sex and recombination provide the variation for the natural selection to act upon is dominated in most discussions of the biological meaning of the sexual reproduction. Here, the idea is substantiated that the main advantage of sex is the opposite: the ability to counteract not only extinction but further evolution as well. Living systems live long owing to their ability to reproduce themselves with a high fidelity. Simple organisms (like bacteria) reach the continued existence due to the high fidelity of individual genome replication. In organisms with a large genome and complex development, the achievable fidelity of DNA replication is not enough for the precise reproduction of the genome. Such species must be capable of surviving and must remain unchanged in spite of the continuous changes of their genes. This problem has no solution in the frame of asexual ("homeogenomic") lineages. They would rapidly degrade and become extinct or blurred out in the course of the reckless evolution. The core outcome of the transition to sexual reproduction was the creation of multiorganismic entity - biological species. Individual organisms forfeited their ability to reproduce autonomously. It implies that individual organisms forfeited their ability to substantive evolution. They evolve as a part of the biological species. In case of obligatory sexuality, there is no such a thing as synchronic multi-level selection. Natural selection cannot select anything that is not a unit of reproduction. Hierarchy in biology implies the functional predestination of the parts for the sake of the whole. A crucial feature of the sexual reproduction is the formation of genomes of individual organisms by random picking them over from the continuously shuffled gene pool instead of the direct replication of the ancestor's genome. A clear anti-evolutionary consequence of the sexuality is evident from the fact that the genotypes of the individuals with an enhanced competitiveness are not transmitted to the next generation. Instead, after mating with "ordinary" individuals, these genotypes scatter and rearrange in new gene combinations, thus preventing the winner from exploiting the success.     

Genetic tests of ancient asexuality in Root Knot Nematodes reveal recent hybrid origins

Background  

The existence of "ancient asexuals", taxa that have persisted for long periods of evolutionary history without sexual recombination, is both controversial and important for our understanding of the evolution and maintenance of sexual reproduction. A lack of sex has consequences not only for the ecology of the asexual organism but also for its genome. Several genetic signatures are predicted from long-term asexual (apomictic) reproduction including (i) large "allelic" sequence divergence (ii) lack of phylogenetic clustering of "alleles" within morphological species and (iii) decay and loss of genes specific to meiosis and sexual reproduction. These genetic signatures can be hard to assess since it is difficult to demonstrate the allelic nature of very divergent sequences, divergence levels may be complicated by processes such as inter-specific hybridization, and genes may have secondary roles unrelated to sexual reproduction. Apomictic species of Meloidogyne root knot nematodes have been suggested previously to be ancient asexuals. Their relatives reproduce by meiotic parthenogenesis or facultative sexuality, which in combination with the abundance of nematode genomic sequence data, makes them a powerful system in which to study the consequences of reproductive mode on genomic divergence.     

Evolution of sex: role of deleterious mutation and mobile elements

Prevalence of sexual reproduction is still enigma. The main character of sex is alleles mixing that could be advantageous either in unstable environment (in this case sex provides high temp of evolution) or in unstable genotype (in this case sex provides purge of genome from deleterious mutations). As long as not all species inhabit highly changeable environments, variation of genotypes is more important factor. As the majority of new mutations is deleterious, effective mechanism of genome purging is needed. Maintenance of "purging mechanism" may be a single role of sex. Two promising mutational hypotheses--clade selection (Muller's ratchet and Nunney's hypothesis) and mutational deterministic hypothesis of Kondrashov claim that more effective elimination of slightly-deleterious mutations provides main advantage to sexual population in comparison with asexual. Despite prima facie similarity, these hypotheses differ in mechanisms, work at different temporal scales and have different consequences. Kondrashov's hypothesis reveals short-term advantage of sexual reproduction, and thus, based on the individual selection. Clade selection displays long-term advantage of sexual reproduction that could be realized only by group selection. The role of mobile elements in evolution of sexual reproduction is also discussed. Firstly, mobile elements ("sexual molecular parasites") can complicate the problem: having been domesticated in asexual genomes and remaining active in sexual genomes they lead to higher mutational rate in sexual organisms and so violate assumption critical for both mutational hypotheses of "other things being equal". Secondly, mobile elements could be leader factor of origin of sex (hypothesis proposed by Hickey). Because theory of group selection could explain maintenance of sex, but not its origin, mobile elements could induce the origin of sex but were not able to maintain it, so the next scenario of evolution of sex is proposed: mobile elements induced origin of sex, which was established later by group selection because provided long term benefit (Muller's ratchet and Nunney's hypothesis). So, on all stages of evolution, sex was not advantageous for the organism per se.     

Mating system shifts and transposable element evolution in the plant genus Capsella

Background

Despite having predominately deleterious fitness effects, transposable elements (TEs) are major constituents of eukaryote genomes in general and of plant genomes in particular. Although the proportion of the genome made up of TEs varies at least four-fold across plants, the relative importance of the evolutionary forces shaping variation in TE abundance and distributions across taxa remains unclear. Under several theoretical models, mating system plays an important role in governing the evolutionary dynamics of TEs. Here, we use the recently sequenced Capsella rubella reference genome and short-read whole genome sequencing of multiple individuals to quantify abundance, genome distributions, and population frequencies of TEs in three recently diverged species of differing mating system, two self-compatible species (C. rubella and C. orientalis) and their self-incompatible outcrossing relative, C. grandiflora.

Results

We detect different dynamics of TE evolution in our two self-compatible species; C. rubella shows a small increase in transposon copy number, while C. orientalis shows a substantial decrease relative to C. grandiflora. The direction of this change in copy number is genome wide and consistent across transposon classes. For insertions near genes, however, we detect the highest abundances in C. grandiflora. Finally, we also find differences in the population frequency distributions across the three species.

Conclusion

Overall, our results suggest that the evolution of selfing may have different effects on TE evolution on a short and on a long timescale. Moreover, cross-species comparisons of transposon abundance are sensitive to reference genome bias, and efforts to control for this bias are key when making comparisons across species.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-602) contains supplementary material, which is available to authorized users.     

Molecular evolution under increasing transposable element burden in <Emphasis Type="Italic">Drosophila</Emphasis>: A speed limit on the evolutionary arms race

Background

Genome architecture is profoundly influenced by transposable elements (TEs), and natural selection against their harmful effects is a critical factor limiting their spread. Genome defense by the piRNA silencing pathway also plays a crucial role in limiting TE proliferation. How these two forces jointly determine TE abundance is not well understood. To shed light on the nature of factors that predict TE success, we test three distinct hypotheses in the Drosophila genus. First, we determine whether TE abundance and relaxed genome-wide purifying selection on protein sequences are positively correlated. This serves to test the hypothesis that variation in TE abundance in the Drosophila genus can be explained by the strength of natural selection, relative to drift, acting in parallel against mildly deleterious non-synonymous mutations. Second, we test whether increasing TE abundance is correlated with an increased rate of amino-acid evolution in genes encoding the piRNA machinery, as might be predicted by an evolutionary arms race model. Third, we test whether increasing TE abundance is correlated with greater codon bias in genes of the piRNA machinery. This is predicted if increasing TE abundance selects for increased efficiency in the machinery of genome defense.

Results

Surprisingly, we find neither of the first two hypotheses to be true. Specifically, we found that genome-wide levels of purifying selection, measured by the ratio of non-synonymous to synonymous substitution rates (ω), were greater in species with greater TE abundance. In addition, species with greater TE abundance have greater levels of purifying selection in the piRNA machinery. In contrast, it appears that increasing TE abundance has primarily driven adaptation in the piRNA machinery by increasing codon bias.

Conclusions

These results indicate that within the Drosophila genus, a historically reduced strength of selection relative to drift is unlikely to explain patterns of increased TE success across species. Other factors, such as ecological exposure, are likely to contribute to variation in TE abundances within species. Furthermore, constraints on the piRNA machinery may temper the evolutionary arms race that would drive increasing rates of evolution at the amino acid level. In the face of these constraints, selection may act primarily by improving the translational efficiency of the machinery of genome defense through efficient codon usage.

     

Clonal reproduction shapes evolution in the lizard malaria parasite Plasmodium floridense

The preponderant clonal evolution hypothesis (PCE) predicts that frequent clonal reproduction (sex between two clones) in many pathogens capable of sexual recombination results in strong linkage disequilibrium and the presence of discrete genetic subdivisions characterized by occasional gene flow. We expand on the PCE and predict that higher rates of clonal reproduction will result in: (1) morphologically cryptic species that exhibit (2) low within‐species variation and (3) recent between‐species divergence. We tested these predictions in the Caribbean lizard malaria parasite Plasmodium floridense using 63 single‐infection samples in lizards collected from across the parasite's range, and sequenced them at two mitochondrial, one apicoplast, and five nuclear genes. We identified 11 provisionally cryptic species within P. floridense, each of which exhibits low intraspecific variation and recent divergence times between species (some diverged approximately 110,000 years ago). Our results are consistent with the hypothesis that clonal reproduction can profoundly affect diversification of species capable of sexual recombination, and suggest that clonal reproduction may have led to a large number of unrecognized pathogen species. The factors that may influence the rates of clonal reproduction among pathogens are unclear, and we discuss how prevalence and virulence may relate to clonal reproduction.     

The evolution of transposable elements in natural populations of self-fertilizing <Emphasis Type="Italic">Arabidopsis thaliana</Emphasis> and its outcrossing relative <Emphasis Type="Italic">Arabidopsis lyrata</Emphasis>

Background  

Transposable Elements (TEs) make up the majority of plant genomes, and thus understanding TE evolutionary dynamics is key to understanding plant genome evolution. Plant reproductive systems are diverse and mating type variation is one factor among many hypothesized to influence TE evolutionary dynamics. Here, we collected a large TE-display data set in self-fertilizing Arabidopsis thaliana, and compared it to data gathered in outcrossing Arabidopsis lyrata. We analyzed seven TE families in four natural populations of each species to tease apart the effects of mating system, demography, transposition, and selection in determining patterns of TE diversity.     

TERAD: Extraction of transposable element composition from RADseq data

Transposable elements (TEs) – selfish DNA sequences that can move within the genome – comprise a large proportion of the genomes of many organisms. Although low‐coverage whole‐genome sequencing can be used to survey TE composition, it is noneconomical for species with large quantities of DNA. Here, we utilize restriction‐site associated DNA sequencing (RADSeq) as an alternative method to survey TE composition. First, we demonstrate in silico that double digest restriction‐site associated DNA sequencing (ddRADseq) markers contain the same TE compositions as whole genome assemblies across arthropods. Next, we show empirically using eight Synalpheus snapping shrimp species with large genomes that TE compositions from ddRADseq and low‐coverage whole‐genome sequencing are comparable within and across species. Finally, we develop a new bioinformatic pipeline, TERAD, to extract TE compositions from RADseq data. Our study expands the utility of RADseq to study the repeatome, making comparative studies of genome structure for species with large genomes more tractable and affordable.     

Divergent genome sizes reflect the infrafamilial subdivision of the neotropical woody Marcgraviaceae

Neotropical Marcgraviaceae comprise about seven genera and 130 species of lianas and shrubs. They predominantly occur in lowland or montane rainforests and are characterized by a variety of pollination systems. Early classifications subdivided Marcgraviaceae into subfamilies Marcgravioideae and Noranteoideae, a concept supported by molecular data. Using flow cytometry and chromosome numbers, we investigated the role of genome size and polyploidization in the evolution of Marcgraviaceae and how genome sizes are distributed between the proposed infrafamilial groups. To do this we determined genome sizes and chromosome counts for six genera and 22 species for the first time. Our study supports the subfamilial classification of the family, revealing contrasting genome sizes in Noranteoideae (2C = 5.5–21.5 pg) and Marcgravioideae (2C = 2.3–6.2 pg). Polyploidy is considered to be the main source of genome size variation as in each subfamily the higher nuclear DNA amounts were associated with higher ploidy. In addition, genome size changes independent of polyploidy were also observed in some genera, suggesting an additional role for changes in repetitive DNA abundance in the evolution of Marcgraviaceae. A high chromosome base number (x = 18; 2n = 36 to ～70) points to an undetected lower diploid level or to palaeopolyploidy. Marcgraviaceae show a remarkable (nine‐fold) variation in genome size, and several Noranteoideae have genome sizes among the highest reported for tropical woody angiosperms worldwide. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177 , 1–14.     

Selection of low investment in sex in a cyclically parthenogenetic rotifer

Cyclical parthenogens, which combine asexual and sexual reproduction, are good models for research into the ecological and population processes affecting the evolutionary maintenance of sex. Sex in cyclically parthenogenetic rotifers is necessary for diapausing egg production, which is essential to survive adverse conditions between planktonic growing seasons. However, within a planktonic season sexual reproduction prevents clonal proliferation. Hence, clones with a low propensity for sex should be selected, becoming dominant in the population as the growing season progresses. In this context, we studied the dynamics of the heritable variation in propensity for sexual reproduction among clones of a Brachionus plicatilis rotifer population in a temporary Mediterranean pond during the period the species occurred in plankton. Clonal isolates displayed high heritable variation in their propensity for sex. Moreover, the frequency of clones with low propensity for sex increased during the growing season, which supports the hypothesized short‐term selection for low investment in sex within a growing season. These results demonstrate (1) the inherent instability of the cyclical parthenogenetic life cycle, (2) the cost of sexual reproduction in cyclical parthenogens where sex produces diapausing eggs and (3) the role of the association between sexual reproduction and diapause in maintaining sex in these cyclical parthenogens.     

Evolutionary transitions in the Asteraceae coincide with marked shifts in transposable element abundance

Background

The transposable element (TE) content of the genomes of plant species varies from near zero in the genome of Utricularia gibba to more than 80 % in many species. It is not well understood whether this variation in genome composition results from common mechanisms or stochastic variation. The major obstacles to investigating mechanisms of TE evolution have been a lack of comparative genomic data sets and efficient computational methods for measuring differences in TE composition between species. In this study, we describe patterns of TE evolution in 14 species in the flowering plant family Asteraceae and 1 outgroup species in the Calyceraceae to investigate phylogenetic patterns of TE dynamics in this important group of plants.

Results

Our findings indicate that TE families in the Asteraceae exhibit distinct patterns of non-neutral evolution, and that there has been a directional increase in copy number of Gypsy retrotransposons since the origin of the Asteraceae. Specifically, there is marked increase in Gypsy abundance at the origin of the Asteraceae and at the base of the tribe Heliantheae. This latter shift in genome composition has had a significant impact on the diversity and abundance distribution of TEs in a lineage-specific manner.

Conclusions

We show that the TE-driven expansion of plant genomes can be facilitated by just a few TE families, and is likely accompanied by the modification and/or replacement of the TE community. Importantly, large shifts in TE composition may be correlated with major of phylogenetic transitions.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-1830-8) contains supplementary material, which is available to authorized users.     

Female‐biased size dimorphism in a diapausing caddisfly,Mesophylax aspersus: effect of fecundity and natural and sexual selection

1. The effect of mating success, female fecundity and survival probability associated with intra‐sex variation in body size was studied in Mesophylax aspersus, a caddisfly species with female‐biased sexual size dimorphism, which inhabits temporary streams and aestivates in caves. Adults of this species do not feed and females have to mature eggs during aestivation. 2. Thus, females of larger size should have a fitness advantage because they can harbour more energy reserves that could influence fecundity and probability of survival until reproduction. In contrast, males of smaller size might have competitive advantages over others in mating success. 3. These hypotheses were tested by comparing the sex ratio and body size of individuals captured before and after the aestivation period. The associations between body size and female fecundity, and between mating success and body size of males, were explored under laboratory conditions. 4. During the aestivation period, the sex ratio changed from 1 : 1 to male biased (4 : 1), and a directional selection on body size was detected for females but not for males. Moreover, larger clutches were laid by females of larger size. Finally, differences in mating success between small and large males were not detected. These results suggest that natural selection (i.e. the differential mortality of females associated with body size) together with possible fecundity advantages, are important factors responsible of the sexual size dimorphism of M. aspersus. 5. These results highlight the importance of taking into account mechanisms other than those traditionally used to explain sexual dimorphism. Natural selection acting on sources of variation, such as survival, may be as important as fecundity and sexual selection in driving the evolution of sexual size dimorphism.     

Current and historical factors drive variation of reproductive traits in unisexual mosses in Europe: A case study

Unisexual bryophytes provide excellent models to study the mechanisms that regulate the frequency of sexual versusasexual reproduction in plants, and their ecological and evolutionary implications. Here, we determined sex expression, phenotypic sex ratio, and individual shoot traits in 242 populations of the cosmopolitan moss Pseudoscleropodium purum spanning its whole distributional range. We tested whether niche differentiation, sex-specific differences in shoot size, and biogeographical history explained the spatial variation of reproductive traits. We observed high levels of sex expression and predominantly female-biased populations, although both traits showed high intraspecific variation among populations. Sex expression and sex ratio were partly explained by current macroscale environmental variation, with male shoots being less frequent at the higher end of the environmental gradients defined by the current distribution of the species. Female bias in population sex ratio was significantly lower in areas recolonized after the last glacial maximum (recent populations) than in glacial refugia (long-term persistent populations). We demonstrated that reproductive trait variation in perennial unisexual mosses is partially driven by macroscale and historical environmental variation. Based on our results, we hypothesize that sexual dimorphism in environmental tolerance and vegetative growth contribute to sex ratio bias over time, constraining the chances of sexual reproduction, especially in long-term persistent populations. Further studies combining genetic analyses and population monitoring should improve our understanding of the implications of the intraspecific variation in the frequency of sexual versusasexual reproduction in bryophyte population fitness and eco-evolutionary dynamics.     

Strong phylogenetic inertia on genome size and transposable element content among 26 species of flies

While the evolutionary mechanisms driving eukaryote genome size evolution are still debated, repeated element content appears to be crucial. Here, we reconstructed the phylogeny and identified repeats in the genome of 26 Drosophila exhibiting a twofold variation in genome size. The content in transposable elements (TEs) is highly correlated to genome size evolution among these closely related species. We detected a strong phylogenetic signal on the evolution of both genome size and TE content, and a genome contraction in the Drosophila melanogaster subgroup.     

Sex allocation in a simultaneous hermaphrodite, the zebra goby Lythrypnus zebra: insights gained through a comparison with its sympatric congener, Lythrypnus dalli

Synopsis The sexual pattern of the zebra goby Lythrypnus zebra, is an apparent exception to sex allocation theory. Most L. zebra are simultaneous hermaphrodites (i.e., have active female and male gonadal tissue), yet it appears they do not reproduce as males and females simultaneously. Understanding the maintenance of simultaneous hermaphroditism in L. zebra could expand sex allocation theory. In this study, I used a comparison with the blue-banded goby, Lythrypnus dalli, a sympatric congener with a qualitatively similar sexual pattern, to investigate the role of male spawning rate, body size and sexual flexibility in determining the sexual pattern of L. zebra and to isolate differences between the species that might explain their differing sexual patterns. Using field measurements of male nesting success, I found no differences between the species in the body size of nesting males suggesting that large size is associated with successful male reproduction in both species. In addition, nesting males spawned at approximately three times the rate of females in both species; thus, reproduction via male function can be equally advantageous relative to adopting the female role. However, the nest longevity of L. zebra males was shorter than that of L. dalli males, suggesting reproduction via male function may be less reliable in L. zebra. Finally, under laboratory conditions, L. zebra females tended to prefer large mates, and L. zebra were able to re-allocate in both directions, exhibiting a greater capacity to switch than L. dalli. Given these results, I suggest that switching between the sexes plays a greater role in maintaining simultaneous hermaphroditism in L. zebra than L. dalli, perhaps because male reproduction is not as consistent in L. zebra. Sexual flexibility may be an important factor affecting patterns of sex allocation, generally.