Evolution of sex: The costs and benefits of sex: new insights from old asexual lineages

Discussions that are aimed at understanding the maintenance of sexual reproduction are in a bit of a quagmire owing to the many competing theories that have been proposed. Also, one of the central observations that asexual lineages are typically short lived still needs to be properly quantified. Exciting new results on ancient asexual organisms show that lineages can persist for many millions of generations without recombination. Understanding how they do so might well provide crucial new insights into the problem of sex.     

Admixed sexual and facultatively asexual aphid lineages at mating sites

Cyclically parthenogenetic organisms may have facultative asexual counterparts. Such organisms, including aphids, are therefore interesting models for the study of ecological and genetic interactions between lineages differing in reproductive mode. Earlier studies on aphids have revealed major differences in the genetic outcomes of populations that are possibly resulting mostly either from sexual or from asexual reproduction. Besides, notable gene flow between sexual and asexual derivatives has been suspected, which could lead to the emergence of new asexual lineages. The present study examines the interplay between these lineages and is based on analyses of population structure of individuals that may contribute to the pool of sexual reproductive forms in the host alternating aphid Rhopalosiphum padi. Using a Bayesian assignment method, we first show that the sexual forms of R. padi on mating sites encompass two genetically distinct clusters of individuals in the western part of France. The first cluster included unique genotypes of sexual lineages, while the second cluster included facultatively asexual lineages in numerous copies, the reproductive mode of the two clusters being confirmed by reference clones. Sexual reproductive forms produced by sexual and facultatively asexual lineages are thus admixed at mating sites which gives a large opportunity for the two clusters to mate with each other. Nevertheless, this study also highlights, as previously demonstrated, that the two clusters retained high genetic differentiation. Possible explanations for the inferred limited genetic exchanges are advanced in the discussion, but further dedicated investigations are required to solve this paradox.     

Clonal turnover versus clonal decay: a null model for observed patterns of asexual longevity, diversity and distribution

Phylogenetic and phylogeographic studies suggest that a majority of asexual organisms are evolutionarily recent offshoots of extant sexual taxa and that old clonal lineages tend to be isolated from their sexual and younger asexual counterparts. These observations have often been interpreted as support for the long-term disadvantages of asexuality resulting from the mechanisms of clonal decay. Although clonal decay is likely to be an important mechanism that limits the temporal and spatial distribution of asexual lineages, we argue here that contemporary phylogenetic analyses, which are mostly restricted to simple comparisons of "recent" and "ancient" clones, need to be tested against an appropriate null model of neutrality. We use computer simulations to show that many empirical observations of the distribution of asexuality do not in fact reject a null model of the neutral turnover of clones spawned by sexual relatives. In particular, neutral clonal turnover results in qualitatively similar pattern of clonal spatial distribution and age structure, as does a process that includes clonal decay. Although there are important quantitative differences between predictions made by the two models, we show that published empirical data are still inadequate to distinguish between them. Further work on sexual-asexual complexes is therefore required before clonal turnover can be rejected as a parsimonious explanation of the spatial distribution and age structure of asexual lineages.     

Heterozygosity, Heteromorphy, and Phylogenetic Trees in Asexual Eukaryotes

Little attention has been paid to the consequences of long-term asexual reproduction for sequence evolution in diploid or polyploid eukaryotic organisms. Some elementary theory shows that the amount of neutral sequence divergence between two alleles of a protein-coding gene in an asexual individual will be greater than that in a sexual species by a factor of 2tu, where t is the number of generations since sexual reproduction was lost and u is the mutation rate per generation in the asexual lineage. Phylogenetic trees based on only one allele from each of two or more species will show incorrect divergence times and, more often than not, incorrect topologies. This allele sequence divergence can be stopped temporarily by mitotic gene conversion, mitotic crossing-over, or ploidy reduction. If these convergence events are rare, ancient asexual lineages can be recognized by their high allele sequence divergence. At intermediate frequencies of convergence events, it will be impossible to reconstruct the correct phylogeny of an asexual clade from the sequences of protein coding genes. Convergence may be limited by allele sequence divergence and heterozygous chromosomal rearrangements which reduce the homology needed for recombination and result in aneuploidy after crossing-over or ploidy cycles.     

Multiple losses of sex within a single genus of Microsporidia

Background  

Most asexual eukaryotic lineages have arisen recently from sexual ancestors and contain few ecologically distinct species, providing evidence for long-term advantages of sex. Ancient asexual lineages provide rare exceptions to this rule and so can yield valuable information relating to the evolutionary forces underlying the maintenance of sex. Microsporidia are parasitic, unicellular fungi. They include many asexual species which have traditionally been grouped together into large, presumably ancient taxonomic groups. However, these putative ancient asexual lineages have been identified on the basis of morphology, life cycles and small subunit ribosomal RNA (16S rRNA) gene sequences, all of which hold questionable value in accurately inferring phylogenetic relationships among microsporidia.     

Shifting from clonal to sexual reproduction in aphids: physiological and developmental aspects

Developmental biology is one of the fastest growing and fascinating research fields in life sciences. Among the wide range of embryonic development, a fundamental difference exists between organisms with sexual or asexual development. Aphids are unusual organisms which display alternative pathways of sexual and asexual development, the orientation of the pathway being determined by environmental conditions. These insects offer an adapted system in which to study developmental plasticity, because a side-by-side comparison of sexual and asexual development can be made in individuals with the same genotype. In this review, we describe the developmental mechanisms that have evolved in aphids for alternative sexual and asexual reproduction. In particular, we discuss how environmental cues orientate the reproductive mode of aphids from signal perception to endocrine regulation, and propose a comparative analysis of sexual and asexual gametogenesis and embryogenesis, which has been possible due to the development of molecular methods. As a result of the recent development of genomic resources in aphids, we expect these species will permit major advances in the study of the genomic basis underlying the choice of developmental fate and multiple reproduction strategies.     

Elastic,not plastic species: Frozen plasticity theory and the origin of adaptive evolution in sexually reproducing organisms

Background  

Darwin's evolutionary theory could easily explain the evolution of adaptive traits (organs and behavioral patterns) in asexual but not in sexual organisms. Two models, the selfish gene theory and frozen plasticity theory were suggested to explain evolution of adaptive traits in sexual organisms in past 30 years.     

Imitating the cost of males: A hypothesis for coexistence of all‐female sperm‐dependent species and their sexual host

All‐female sperm‐dependent species are particular asexual organisms that must coexist with a closely related sexual host for reproduction. However, demographic advantages of asexual over sexual species that have to produce male individuals could lead both to extinction. The unresolved question of their coexistence still challenges and fascinates evolutionary biologists. As an alternative hypothesis, we propose those asexual organisms are afflicted by a demographic cost analogous to the production of males to prevent exclusion of the host. Previously proposed hypotheses stated that asexual individuals relied on a lower fecundity than sexual females to cope with demographic advantage. In contrast, we propose that both sexual and asexual species display the same number of offspring, but half of asexual individuals imitate the cost of sex by occupying ecological niches but producing no offspring. Simulations of population growth in closed systems under different demographic scenarios revealed that only the presence of nonreproductive individuals in asexual females can result in long‐term coexistence. This hypothesis is supported by the fact that half of the females in some sperm‐dependent organisms did not reproduce clonally.     

Telomerase deficiency in a colonial ascidian after prolonged asexual propagation

In organisms that propagate by agametic cloning, the parental body is the reproductive unit and fitness increases with clonal size, so that colonial metazoans, despite lack of experimental data, have been considered potentially immortal. Using asexual propagation rate as a measure of somatic performance, and telomerase activity and relative telomere length as molecular markers of senescence, old (7-12 years) asexual strains of a colonial ascidian, Diplosoma listerianum, were compared with their recent sexually produced progeny. We report for the first time evidence for long-term molecular senescence in asexual lineages of a metazoan, and that only passage between sexual generations provides total rejuvenation permitting indefinite propagation and growth. Thus, this colonial ascidian has not fully escaped ageing. The possibility of somatic replicative senescence also potentially helps to explain why metazoans, with the capacity for asexual propagation through agametic cloning, commonly undergo cycles of sexual reproduction in the wild.     

Evolution of clonality and polyploidy in a weevil system

The increased interest in asexual organisms calls for in-depth studies of asexual complexes that actively give rise to new clones. We present an extensive molecular study of the Otiorhynchus scaber (Coleoptera, Curculionidae) weevil system. Three forms have traditionally been recognized: diploid sexuals, triploid, and tetraploid parthenogens. All forms coexist in a small central area, but only the polyploid parthenogens have colonized marginal areas. Analyzing the phylogenetic relationship, based on three partial mitochondrial genes, of 95 individuals from 19 populations, we find that parthenogenesis and polyploidy have originated at least three times from different diploid lineages. We observe two major mitochondrial lineages, with over 2.5% sequence divergence between the most basal groups within them, and find that current distribution and phylogenetic relationships are weakly correlated. Quite unexpectedly, we also discover diploid clones that coexist with, and are morphologically indistinguishable from, the diploid sexual females. Our results support that these diploid clones are derived directly from the diploid sexuals. We also find that it is mainly an increase in ploidy level and not the benefits of asexual reproduction that confers to polyploid parthenogens the advantage over their diploid sexual relatives.     

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.     

General environmental heterogeneity as the explanation of sexuality? Comparative study shows that ancient asexual taxa are associated with both biotically and abiotically homogeneous environments

Ecological theories of sexual reproduction assume that sexuality is advantageous in certain conditions, for example, in biotically or abiotically more heterogeneous environments. Such theories thus could be tested by comparative studies. However, the published results of these studies are rather unconvincing. Here, we present the results of a new comparative study based exclusively on the ancient asexual clades. The association with biotically or abiotically homogeneous environments in these asexual clades was compared with the same association in their sister, or closely related, sexual clades. Using the conservative definition of ancient asexuals (i.e., age >1 million years), we found eight pairs of taxa of sexual and asexual species, six differing in the heterogeneity of their inhabited environment on the basis of available data. The difference between the environmental type associated with the sexual and asexual species was then compared in an exact binomial test. The results showed that the majority of ancient asexual clades tend to be associated with biotically, abiotically, or both biotically and abiotically more homogeneous environments than their sexual controls. In the exploratory part of the study, we found that the ancient asexuals often have durable resting stages, enabling life in subjectively homogeneous environments, live in the absence of intense biotic interactions, and are very often sedentary, inhabiting benthos, and soil. The consequences of these findings for the ecological theories of sexual reproduction are discussed.     

Coalescence times and the Meselson effect in asexual eukaryotes

In asexual eukaryotes, the two allelic gene copies at a locus are expected to become highly divergent as a result of the independent accumulation of mutations in the absence of segregation. If sexual reproduction was abandoned millions of generations ago, intra-individual allelic divergences can be significantly larger than in species that reproduce sexually. Owing to the disputed existence of truly ancient asexual species, this so-called 'Meselson effect' has been put forward as a means of confirming the complete loss of sexual reproduction. Very few attempts have, however, been made at quantifying the effect of sexual reproduction on the degree of divergence between gene copies in an asexual population. Here, I describe how asexual reproduction can be regarded as a special case of population subdivision. Using a slightly modified version of the standard two-deme structured coalescent, I derive the expected coalescence time for a pair of gene copies in an asexual population and show that the Meselson effect is compatible with low rates of sexual reproduction.     

Allelic and genotypic diversity in long-term asexual populations of the pea aphid, Acyrthosiphon pisum in comparison with sexual populations

Many aphid species exhibit geographical variation in the mode of reproduction that ranges from cyclical parthenogenesis with a sexual phase to obligate parthenogenesis (asexual reproduction). Theoretical studies predict that organisms reproducing asexually should maintain higher allelic diversity per locus but lower genotypic diversity than organisms reproducing sexually. To corroborate this hypothesis, we evaluated genotypic and allelic diversities in the sexual and asexual populations of the pea aphid, Acyrthosiphon pisum (Harris). Microsatellite analysis revealed that populations in central Japan are asexual, whereas populations in northern Japan are obligatorily sexual. No mixed populations were detected in our study sites. Phylogenetic analysis using microsatellite data and mitochondrial cytochrome oxidase subunit I (COI) gene sequences revealed a long history of asexuality in central Japan and negated the possibility of the recent origin of the asexual populations from the sexual populations. Asexual populations exhibited much lower genotypic diversity but higher allelic richness per locus than did sexual populations. Asexual populations consisted of a few predominant clones that were considerably differentiated from one another. Sexual populations on alfalfa, an exotic plant in Japan, were most closely related to asexual populations associated with Vicia sativa L. The alfalfa-associated sexual populations harboured one COI haplotype that was included in the haplotype clade of the asexual populations. Available evidence suggests that the sexuality of the alfalfa-associated populations has recently been restored through the northward migration and colonization of alfalfa by V. sativa- associated lineages. Therefore, our results support the theoretical predictions and provide a new perspective on the origin of sexual populations.     

From asexual to eusocial reproduction by multilevel selection by density-dependent competitive interactions

A game theoretical model is developed to illustrate that multilevel selection by density-dependent competitive interactions in mobile organisms might have played a major role in the evolutionary transitions from asexual over sexual to eusocial reproduction. The model has four equilibria with selection occurring among interacting units of respectively one, two, three, and up to infinitely many individuals. The different equilibria are characterised by different levels of competitive interactions among interacting units, and these levels select for different levels of sexual and co-operative reproduction among the individuals of the units. The model predicts: (i) that low-energy organisms with negligible body masses have asexual reproduction; (ii) that high-energy organisms with non-negligible body masses in evolutionary equilibria have sexual reproduction between a female and a male; (iii) that high-energy organisms with non-negligible body masses that increase exponentially at an evolutionary steady state have co-operative reproduction between a sexual pair and a single sexually produced offspring; and (iv) that high-energy organisms with upward constrained body masses have eusocial reproduction between a sexual pair and up to an infinite number of sexually produced offspring workers.     

Evolution in the slow lane: molecular rates of evolution in sexual and asexual ostracods (Crustacea: Ostracoda)

Parthenogenetic lineages within non-marine ostracods can occur either in mixed (with sexual and asexual females) or exclusively asexual taxa. The former mode of reproduction is associated with a high intraspecific diversity at all levels (genetic, morphological, ecological) and, at least in the Cypridoidea, with geographical parthenogenesis. Obligate asexuality is restricted to the Darwinuloidea, the strongest candidate for an ancient asexual animal group after the bdelloid rotifers, and is characterized by low diversity. We have compared rates of molecular evolution for the nuclear ITS1 region and the mitochondrial COI gene amongst the three major lineages of non-marine ostracods with sexual, mixed and asexual reproduction. Absolute rates of molecular evolution are low for both regions in the darwinulids. The slow-down of evolution in ITS1 that has been observed for Darwinula stevensoni (Brady & Robertson) apparently does not occur in other darwinulid species. ITS1 evolves more slowly than COI within non-marine ostracod families, including the darwinulids, but not between superfamilies. The ancient asexuals might have a higher relative substitution rate in ITS1, as would be expected from hypotheses that predict the accumulation of mutations in asexuals. However, the speed-up of ITS could also be ancient, for example through the stochastic loss of most lineages within the superfamily after the Permian–Triassic mass extinction. In this case, the difference in rate would have occurred independently from any effects of asexual reproduction.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 93–100.     

Escape from the Red Queen: an overlooked scenario in coevolutionary studies

Almost all eukaryotic organisms undergo sexual recombination at some stage of their life history. However, strictly asexual organisms should have higher per capita rate of reproduction compared with those that have sex, so the latter must convey some advantage which overrides the reproductive benefit of asexuality. For example, sexual reproduction and recombination may play an important role in allowing organisms to evolutionarily ‘keep up’ with parasites. Host–parasite coevolution can operate via negative frequency‐dependent selection whereby parasite genotypes adapt to infect host genotypes as they become locally common. By producing more genetically diverse offspring with unique genotypes, sexual organisms have an advantage over asexual counterparts. Essentially, sexual hosts are more difficult for coevolving parasites to ‘track’ over time. This scenario has been named the “Red Queen hypothesis”. It refers to a passage in Lewis Carroll's ‘Through the Looking Glass’ in which the Red Queen tells Alice: ‘it takes all the running you can do, to keep in the same place’; this statement resembles the negative frequency‐dependent dynamics of host–parasite coevolution.     

A general purpose genotype in an ancient asexual

Many parthenogenetic species are geographically more widely distributed than their sexual relatives. Their success has been partly attributed to the existence of general purpose genotypes (GPGs). Darwinula stevensoni is an ostracod species, which has persisted for >25 million years without sex, and is both ubiquitous and cosmopolitan. Here, we test the hypothesis that this ancient asexual species may possess a highly generalised (or general purpose) genotype. The ecological tolerance of D. stevensoni was compared with asexual populations of Heterocypris incongruens, a common cypridinid species with mixed reproduction, as well as with that of another ancient asexual darwinulid species with a limited geographic and ecological distribution, Vestalenula molopoensis. The unusually wide tolerance range for both salinity (0-30 g/l) and temperature (10°C, 20°C and 30°C) of the freshwater species D. stevensoni, supports the hypothesis that this ancient asexual has indeed developed a GPG. This coincides with its wide geographic and ecological distribution and might explain its persistence as an obligate asexual in its long-term evolution. The more restricted salinity tolerance of V. molopoensis (maximum at 12 g/l) shows that not all species of the ancient asexual family Darwinulidae have a GPG. D. stevensoni has a much broader tolerance than the asexuals of H. incongruens. We argue why a GPG is most likely to develop in long-term asexuals.     

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.     

Independently evolving species in asexual bdelloid rotifers

Asexuals are an important test case for theories of why species exist. If asexual clades displayed the same pattern of discrete variation as sexual clades, this would challenge the traditional view that sex is necessary for diversification into species. However, critical evidence has been lacking: all putative examples have involved organisms with recent or ongoing histories of recombination and have relied on visual interpretation of patterns of genetic and phenotypic variation rather than on formal tests of alternative evolutionary scenarios. Here we show that a classic asexual clade, the bdelloid rotifers, has diversified into distinct evolutionary species. Intensive sampling of the genus Rotaria reveals the presence of well-separated genetic clusters indicative of independent evolution. Moreover, combined genetic and morphological analyses reveal divergent selection in feeding morphology, indicative of niche divergence. Some of the morphologically coherent groups experiencing divergent selection contain several genetic clusters, in common with findings of cryptic species in sexual organisms. Our results show that the main causes of speciation in sexual organisms, population isolation and divergent selection, have the same qualitative effects in an asexual clade. The study also demonstrates how combined molecular and morphological analyses can shed new light on the evolutionary nature of species.