Habitat heterogeneity favors asexual reproduction in natural populations of grassthrips

Explaining the overwhelming success of sex among eukaryotes is difficult given the obvious costs of sex relative to asexuality. Different studies have shown that sex can provide benefits in spatially heterogeneous environments under specific conditions, but whether spatial heterogeneity commonly contributes to the maintenance of sex in natural populations remains unknown. We experimentally manipulated habitat heterogeneity for sexual and asexual thrips lineages in natural populations and under seminatural mesocosm conditions by varying the number of hostplants available to these herbivorous insects. Asexual lineages rapidly replaced the sexual ones, independently of the level of habitat heterogeneity in mesocosms. In natural populations, the success of sexual thrips decreased with increasing habitat heterogeneity, with sexual thrips apparently only persisting in certain types of hostplant communities. Our results illustrate how genetic diversity‐based mechanisms can favor asexuality instead of sex when sexual lineages co‐occur with genetically variable asexual lineages.     

Multiple routes to asexuality in an aphid species.

Cyclical parthenogens, including aphids, are important models for studying the evolution of sex. However, little is known about transitions to asexuality in aphids, although the mode of origin of asexual lineages has important consequences for their level of genetic diversity, ecological adaptability and the outcome of competition with their sexual relatives. Thus, we surveyed nuclear, mitochondrial and biological data obtained on cyclical and obligate parthenogens of the bird cherry-oat aphid, Rhopalosiphum padi (L), to investigate the frequency of transitions from sexuality to permanent asexuality. Many instances of asexual lineages retaining the ability to produce males are known in aphids, so particular attention was paid to the existence of occasional matings between females from sexual lineages and males produced by asexual lineages, which have the potential to produce new asexual lineages. Phylogenetic inference based on microsatellite and mitochondrial data indicates at least three independent origins of asexuality in R. padi, yielding the strongest evidence to date for multiple origins of asexuality in an aphid. Moreover, several lines of evidence demonstrate that transitions to asexuality result from two mechanisms: a complete spontaneous loss of sex and repeated gene flow from essentially asexual lineages into sexual ones.     

Phylogenetic evidence for hybrid origins of asexual lineages in an aphid species

Understanding the mode of origin of asexuality is central to ongoing debates concerning the evolution and maintenance of sexual reproduction in eukaryotes. This is because it has profound consequences for patterns of genetic diversity and ecological adaptability of asexual lineages, hence on the outcome of competition with sexual relatives both in short and longer terms. Among the possible routes to asexuality, hybridization is a very common mechanism in animals and plants. Aphids present frequent transitions from their ancestral reproductive mode (cyclical parthenogenesis) to permanent asexuality, but the mode of origin of asexual lineages is generally not known because it has never been thoroughly investigated with appropriate molecular tools. Rhopalosiphum padi is an aphid species with coexisting sexual (cyclically parthenogenetic) and asexual (obligately parthenogenetic) lineages that are genetically distinct. Previous studies have shown that asexual lineages of R. padi are heterozygous at most nuclear loci, suggesting either that they have undergone long-term asexuality (under which heterozygosity tends to increase) or that they have hybrid origins. To discriminate between these alternatives, we conducted an extensive molecular survey combining the sequence analysis of alleles of two nuclear DNA markers and mitochondrial DNA haplotypes in sexual and asexual lineages of R. padi. Both nuclear and cytoplasmic markers clearly showed that many asexual lineages have hybrid origins, the first such demonstration in aphids. Our results also indicated that asexuals result from multiple events of hybridization between R. padi and an unknown sibling species, and are of recent origin (contradicting previous estimates that asexual R. padi lineages were of moderate longevity). This study constitutes another example that putatively ancient asexual lineages are actually of much more recent origin than previously thought. It also presents a robust approach for testing whether hybrid origin of asexuality is also a common phenomenon in aphids.     

Genetic Control of Contagious Asexuality in the Pea Aphid

Although evolutionary transitions from sexual to asexual reproduction are frequent in eukaryotes, the genetic bases of such shifts toward asexuality remain largely unknown. We addressed this issue in an aphid species where both sexual and obligate asexual lineages coexist in natural populations. These sexual and asexual lineages may occasionally interbreed because some asexual lineages maintain a residual production of males potentially able to mate with the females produced by sexual lineages. Hence, this species is an ideal model to study the genetic basis of the loss of sexual reproduction with quantitative genetic and population genomic approaches. Our analysis of the co-segregation of ∼300 molecular markers and reproductive phenotype in experimental crosses pinpointed an X-linked region controlling obligate asexuality, this state of character being recessive. A population genetic analysis (>400-marker genome scan) on wild sexual and asexual genotypes from geographically distant populations under divergent selection for reproductive strategies detected a strong signature of divergent selection in the genomic region identified by the experimental crosses. These population genetic data confirm the implication of the candidate region in the control of reproductive mode in wild populations originating from 700 km apart. Patterns of genetic differentiation along chromosomes suggest bidirectional gene flow between populations with distinct reproductive modes, supporting contagious asexuality as a prevailing route to permanent parthenogenesis in pea aphids. This genetic system provides new insights into the mechanisms of coexistence of sexual and asexual aphid lineages.     

Adaptive Significance and Long-Term Survival of Asexual Lineages

Important questions remain about the long-term survival and adaptive significance of eukaryotic asexual lineages. Numerous papers dealing with sex advantages still continued to compare parthenogenetic populations versus sexual populations arguing that sex demonstrates a better fitness. Because asexual lineages do not possess any recombination mechanisms favoring rapid changes in the face of severe environmental conditions, they should be considered as an evolutionary dead-end. Nevertheless, reviewing literature dealing with asexual reproduction, it is possible to draw three stimulating conclusions. (1) Asexual reproduction in eukaryotes considerably differs from prokaryotes which experience recombination but neither meiosis nor syngamy. Recombination and meiosis would be a driving force for sexual reproduction. Eukaryotes should therefore be considered as a continuum of sexual organisms that are more or less capable (and sometimes incapable) of sexual reproduction. (2) Rather than revealing ancestral eukaryotic forms, most known lineages of asexual eukaryotes have lost sex due to a genomic conflict affecting their sexual capacity. Thus, it could be argued that hybridization is a major cause of their asexuality. Asexuality may have evolved as a reproductive mechanism reducing conflict within organisms. (3) It could be proposed that, rather than being generalists, parthenogenetic hybrid lineages could be favored when exploiting peculiar restricted ecological niches, following the “frozen niche variation” model. Although hybrid events may result in sex loss, probably caused by genomic conflict, asexual hybrids could display new original adaptive traits, and the rapid colonization of environments through clonal reproduction could favor their long-term survival, leading to evolutionary changes and hybrid speciation. Examination of the evolutionary history of asexual lineages reveals that evolutionary processes act through transitional stages in which even very small temporary benefits may be enough to counter the expected selective disadvantages.     

Ancient asexual scandals

Asexual organisms that are descended from ancient asexual lineages defy current thinking on the evolution of sexual reproduction; theoreticians have been anxious to explain away their existence. However, a number of groups of organisms, from ferns to rotifers, have been suggested to be anciently asexual, and favourable evidence is being accumulated. Furthermore, new techniques for assessing claims of ancient asexuality have been proposed. Although ancient asexuals challenge current theories of sex, understanding how they manage to persist will help to explain why most organisms are sexual.     

Genomic signatures of ancient asexual lineages

Ancient asexuals – organisms that have lived without sex for millions of years – offer unique opportunities for discriminating among the various theories of the maintenance of sex. The last few years have seen molecular studies of a number of putative ancient asexual lineages, including bdelloid rotifers, Darwinulid ostracods, and mycorrhizal fungi. To help make sense of the diverse findings of such studies, we present a review and classification of the predicted effects of loss of sex on the eukaryotic genome. These include: (1) direct effects on the genetic structure of individuals and populations; (2) direct effects on the mutation rate due to the loss of the sexual phase; (3) decay of genes specific to sex and recombination; (4) effects of the cessation of sexual selection; (5) dis-adaptation due to the reduced efficiency of selection; and (6) adaptations to asexuality. We discuss the utility of the various predictions for detecting ancient asexuality, for testing hypotheses of the reversibility of a transition to asexuality, and for discriminating between theories of sex. In addition, we review the current status of putative ancient asexuals.  © 2003 The Linnean Society of London. Biological Journal of the Linnean Society 2003, 79 , 69–84.     

Twigs on the tree of life? Neutral and selective models for integrating macroevolutionary patterns with microevolutionary processes in the analysis of asexuality

Neutral models characterize evolutionary or ecological patterns expected in the absence of specific causal processes, such as natural selection or ecological interactions. In this study, we describe and evaluate three neutral models that can, in principle, help to explain the apparent 'twigginess' of asexual lineages on phylogenetic trees without involving the negative consequences predicted for the absence of recombination and genetic exchange between individuals. Previously, such phylogenetic twiggyness of asexual lineages has been uncritically interpreted as evidence that asexuality is associated with elevated extinction rates and thus represents an evolutionary dead end. Our first model uses simple phylogenetic simulations to illustrate that, with sexual reproduction as the ancestral state, low transition rates to stable asexuality, or low rates of ascertained 'speciation' in asexuals, can generate twiggy distributions of asexuality, in the absence of high extinction rates for asexual lineages. The second model, developed by Janko et   al . (2008 ), shows that a dynamic equilibrium between origins and neutral losses of asexuals can, under some conditions, generate a relatively low mean age of asexual lineages. The third model posits that the risk of extinction for asexual lineages may be higher than that of sexuals simply because asexuals inhabit higher latitudes or altitudes, and not due to effects of their reproductive systems. Such neutral models are useful in that they allow quantitative evaluation of whether empirical data, such as phylogenetic and phylogeographic patterns of sex and asexuality, indeed support the idea that asexually reproducing lineages persist over shorter evolutionary periods than sexual lineages, due to such processes as mutation accumulation, slower rates of adaptive evolution, or relatively lower levels of genetic variability.     

Lineage Selection and the Maintenance of Sex

Sex predominates in eukaryotes, despite its short-term disadvantage when compared to asexuality. Myriad models have suggested that short-term advantages of sex may be sufficient to counterbalance its twofold costs. However, despite decades of experimental work seeking such evidence, no evolutionary mechanism has yet achieved broad recognition as explanation for the maintenance of sex. We explore here, through lineage-selection models, the conditions favouring the maintenance of sex. In the first model, we allowed the rate of transition to asexuality to evolve, to determine whether lineage selection favoured species with the strongest constraints preventing the loss of sex. In the second model, we simulated more explicitly the mechanisms underlying the higher extinction rates of asexual lineages than of their sexual counterparts. We linked extinction rates to the ecological and/or genetic features of lineages, thereby providing a formalisation of the only figure included in Darwin''s “The origin of species”. Our results reinforce the view that the long-term advantages of sex and lineage selection may provide the most satisfactory explanations for the maintenance of sex in eukaryotes, which is still poorly recognized, and provide figures and a simulation website for training and educational purposes. Short-term benefits may play a role, but it is also essential to take into account the selection of lineages for a thorough understanding of the maintenance of sex.     

Variation in asexual lineage age in Potamopyrgus antipodarum, a New Zealand snail

Asexual lineages are thought to be subject to rapid extinction because they cannot generate recombinant offspring. Accordingly, extant asexual lineages are expected to be of recent derivation from sexual individuals. We examined this prediction by using mitochondrial DNA sequence data to estimate asexual lineage age in populations of a freshwater snail (Potamopyrgus antipodarum) native to New Zealand and characterized by varying frequency of sexual and asexual individuals. We found considerable variation in the amount of genetic divergence of asexual lineages from sexual relatives, pointing to a wide range of asexual lineage ages. Most asexual lineages had close genetic ties (approximately 0.1% sequence divergence) to haplotypes found in sexual representatives, indicating a recent origin from sexual progenitors. There were, however, two asexual clades that were quite genetically distinct (> 1.2% sequence divergence) from sexual lineages and may have diverged from sexual progenitors more than 500,000 years ago. These two clades were found in lakes that had a significantly lower frequency of sexual individuals than lakes without the old clades, suggesting that the conditions that favor sex might select against ancient asexuality. Our results also emphasize the need for large sample sizes and spatially representative sampling when hypotheses for the age of asexual lineages are tested to adequately deal with potential biases in age estimates.     

DO ASEXUAL POLYPLOID LINEAGES LEAD SHORT EVOLUTIONARY LIVES? A CASE STUDY FROM THE FERN GENUS ASTROLEPIS

A life-history transition to asexuality is typically viewed as leading to a heightened extinction risk, and a number of studies have evaluated this claim by examining the relative ages of asexual versus closely related sexual lineages. Surprisingly, a rigorous assessment of the age of an asexual plant lineage has never been published, although asexuality is extraordinarily common among plants. Here, we estimate the ages of sexual diploids and asexual polyploids in the fern genus Astrolepis using a well-supported plastid phylogeny and a relaxed-clock dating approach. The 50 asexual polyploid samples we included were conservatively estimated to comprise 19 distinct lineages, including a variety of auto- and allopolyploid genomic combinations. All were either the same age or younger than the crown group comprising their maternal sexual-diploid parents based simply on their phylogenetic position. Node ages estimated with the relaxed-clock approach indicated that the average maximum age of asexual lineages was 0.4 My, and individual lineages were on average 7 to 47 times younger than the crown- and total-ages of their sexual parents. Although the confounding association between asexuality and polyploidy precludes definite conclusions regarding the effect of asexuality, our results suggest that asexuality limits evolutionary potential in Astrolepis.     

Loss of sexual recombination and segregation is associated with increased diversification in evening primroses

The loss of sexual recombination and segregation in asexual organisms has been portrayed as an irreversible process that commits asexually reproducing lineages to reduced diversification. We test this hypothesis by estimating rates of speciation, extinction, and transition between sexuality and functional asexuality in the evening primroses. Specifically, we estimate these rates using the recently developed BiSSE (Binary State Speciation and Extinction) phylogenetic comparative method, which employs maximum likelihood and Bayesian techniques. We infer that net diversification rates (speciation minus extinction) in functionally asexual evening primrose lineages are roughly eight times faster than diversification rates in sexual lineages, largely due to higher speciation rates in asexual lineages. We further reject the hypothesis that a loss of recombination and segregation is irreversible because the transition rate from functional asexuality to sexuality is significantly greater than zero and in fact exceeded the reverse rate. These results provide the first empirical evidence in support of the alternative theoretical prediction that asexual populations should instead diversify more rapidly than sexual populations because they are free from the homogenizing effects of sexual recombination and segregation. Although asexual reproduction may often constrain adaptive evolution, our results show that the loss of recombination and segregation need not be an evolutionary dead end in terms of diversification of lineages.     

MOLECULAR MARKERS INDICATE RARE SEX IN A PREDOMINANTLY ASEXUAL PARASITOID WASP

The parasitoid wasp genus Lysiphlebus (Hymenoptera: Braconidae: Aphidiinae) contains a taxonomically poorly resolved group of both sexual (arrhenotokous) species and asexual (thelytokous) clones. Maximum-parsimony and maximum-likelihood analyses of mitochondrial DNA sequence data from specimens collected across Western Europe showed that asexuality, which does not appear to be caused by the bacterium Wolbachia, is concentrated in two geographically widespread lineages, the older of which diverged from the closest extant sexual taxa approximately 0.5 million years ago. However, the DNA sequences of a nuclear intron (elongation factor—1α) showed no congruence with this pattern, and a much higher frequency of heterozygotes with very high allelic diversity was observed among the asexual females compared to that among females from the sexual species. This pattern is consistent with maternally inherited asexuality coupled with a history of rare sex with members of several closely related sexual populations or species. Our observations reinforce recent arguments that rare sex may be more important for the persistence of otherwise asexual lineages than hitherto appreciated.     

THE MAINTENANCE OF SEX BY GROUP SELECTION

The traditional group-selection model for the maintenance of sex is based upon the assumption that the long-term evolutionary benefits of sexual reproduction result in asexual lineages having a higher extinction rate than sexual species. This model is reexamined, as is a related model that incorporates the possibility that sexual and asexual lines differ in their speciation rates. In these models, the long-term advantage of sex is opposed by a strong short-term disadvantage arising from the twofold reproductive cost of producing males. It is shown that once some sexual lines become established, then group selection can act to maintain sex despite its short-term disadvantage. The short-term disadvantage is included in the model by assuming that, if asexual individuals arise by mutation within a previously completely sexual species, then the asexuals quickly displace their sexual conspecifics and the species is transformed to asexuality. The probability of this event is given by the transition rate, u_s. If the value of u_s varies between lineages, then one of the effects of group selection is to favor groups (i.e., species) with the lowest values of u_s. This occurs because lines that do convert to asexuality (because of a high u_s) are doomed to a high rate of extinction, and in the long term only those that do not convert to asexuality (because of a low u_s) survive. The net result of group selection is that sex is maintained because of its lower extinction rate (or higher speciation rate) and because asexual mutants only rarely arise.     

Evolutionary traction: the cost of adaptation and the evolution of sex

The advantage of sexual reproduction remains a puzzle for evolutionary biologists. Everything else being equal, asexual populations are expected to have twice the number of offspring produced by similar sexual populations. Yet, asexual species are uncommon among higher eukaryotes. In models assuming small populations, high mutation rates, or frequent environmental changes, sexual reproduction seems to have at least a two-fold advantage over asexuality. But the advantage of sex for large populations, low mutation rates, and rare or mild environmental changes remains a conundrum. Here we show that without recombination, rare advantageous mutations can result in increased accumulation of deleterious mutations ('evolutionary traction'), which explains the long-term advantage of sex under a wide parameter range.     

The maintenance of sexual reproduction in a structured population

We present the results of a computer simulation model in which a sexual population produces an asexual mutant. We estimate the probability that the new asexual lineage will go extinct. We find that whenever the asexual lineage does not go extinct the sexual population is out-competed, and only asexual individuals remain after a sufficiently long period of time has elapsed. We call this type of outcome an asexual takeover. Our results suggest that, given repeated mutations to asexuality, asexual takeover is likely in an unstructured environment. However, if the environment is subdivided into demes that are connected by migration, then asexual takeover becomes less likely. The probability of asexual takeover declines towards zero as the number of demes increases and as the rate of migration decreases. The reason for this is that asexuality leads to a greater loss of fitness due to mutation and genetic drift, in comparison to what occurs under sexual reproduction. Population subdivision slows the spread of asexual lineages, which allows more time for the genetic degeneration caused by asexuality to take place.     

Molecular evidence for ancient asexuality in timema stick insects

Asexuality is rare in animals in spite of its apparent advantage relative to sexual reproduction, indicating that it must be associated with profound costs [1-9]. One expectation is that reproductive advantages gained by new asexual lineages will be quickly eroded over time [3, 5-7]. Ancient asexual taxa that have evolved and adapted without sex would be "scandalous" exceptions to this rule, but it is often difficult to exclude the possibility that putative asexuals deploy some form of "cryptic" sex, or have abandoned sex more recently than estimated from divergence times to sexual relatives [10]. Here we provide evidence, from high intraspecific divergence of mitochondrial sequence and nuclear allele divergence patterns, that several independently derived Timema stick-insect lineages have persisted without recombination for more than a million generations. Nuclear alleles in the asexual lineages displayed significantly higher intraindividual divergences than in related sexual species. In addition, within two asexuals, nuclear allele phylogenies suggested the presence of two clades, with sequences from the same individual appearing in both clades. These data strongly support ancient asexuality in Timema and validate the genus as an exceptional opportunity to attack the question of how asexual reproduction can be maintained over long periods of evolutionary time.     

Can resource costs of polyploidy provide an advantage to sex?

The predominance of sexual reproduction despite its costs indicates that sex provides substantial benefits, which are usually thought to derive from the direct genetic consequences of recombination and syngamy. While genetic benefits of sex are certainly important, sexual and asexual individuals, lineages, or populations may also differ in physiological and life history traits that could influence outcomes of competition between sexuals and asexuals across environmental gradients. Here, we address possible phenotypic costs of a very common correlate of asexuality, polyploidy. We suggest that polyploidy could confer resource costs related to the dietary phosphorus demands of nucleic acid production; such costs could facilitate the persistence of sex in situations where asexual taxa are of higher ploidy level and phosphorus availability limits important traits like growth and reproduction. We outline predictions regarding the distribution of diploid sexual and polyploid asexual taxa across biogeochemical gradients and provide suggestions for study systems and empirical approaches for testing elements of our hypothesis.     

No sex in fungus-farming ants or their crops

Asexual reproduction imposes evolutionary handicaps on asexual species, rendering them prone to extinction, because asexual reproduction generates novel genotypes and purges deleterious mutations at lower rates than sexual reproduction. Here, we report the first case of complete asexuality in ants, the fungus-growing ant Mycocepurus smithii, where queens reproduce asexually but workers are sterile, which is doubly enigmatic because the clonal colonies of M. smithii also depend on clonal fungi for food. Degenerate female mating anatomy, extensive field and laboratory surveys, and DNA fingerprinting implicate complete asexuality in this widespread ant species. Maternally inherited bacteria (e.g. Wolbachia, Cardinium) and the fungal cultivars can be ruled out as agents inducing asexuality. M. smithii societies of clonal females provide a unique system to test theories of parent–offspring conflict and reproductive policing in social insects. Asexuality of both ant farmer and fungal crop challenges traditional views proposing that sexual farmer ants outpace coevolving sexual crop pathogens, and thus compensate for vulnerabilities of their asexual crops. Either the double asexuality of both farmer and crop may permit the host to fully exploit advantages of asexuality for unknown reasons or frequent switching between crops (symbiont reassociation) generates novel ant–fungus combinations, which may compensate for any evolutionary handicaps of asexuality in M. smithii.     

EVALUATION OF ELEVATED PLOIDY AND ASEXUAL REPRODUCTION AS ALTERNATIVE EXPLANATIONS FOR GEOGRAPHIC PARTHENOGENESIS IN EUCYPRIS VIRENS OSTRACODS

Transitions from sexual to asexual reproduction are often coupled with elevations in ploidy. As a consequence, the importance of ploidy per se for the maintenance and spread of asexual populations is unclear. To examine the effects of ploidy and asexual reproduction as independent determinants of the success of asexual lineages, we sampled diploid sexual, diploid asexual, and triploid asexual Eucypris virens ostracods across a European wide range. Applying nuclear and mitochondrial markers, we found that E. virens consists of genetically highly differentiated diploid sexual populations, to the extent that these sexual clades could be considered as cryptic species. All sexual populations were found in southern Europe and North Africa and we found that both diploid asexual and triploid asexual lineages have originated multiple times from several sexual lineages. Therefore, the asexual lineages show a wide variety of genetic backgrounds and very strong population genetic structure across the wide geographic range. Finally, we found that triploid, but not diploid, asexual clones dominate habitats in northern Europe. The limited distribution of diploid asexual lineages, despite their shared ancestry with triploid asexual lineages, strongly suggests that the wider geographic distribution of triploids is due to elevated ploidy rather than to asexuality.