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.     

Sex and adaptation in a changing environment.

In this study we consider a mathematical model of a sexual population that lives in a changing environment. We find that a low rate of environmental change can produce a very large increase in genetic variability. This may help to explain the high levels of heritability observed in many natural populations. We also study asexuality and find that a modest rate of environmental change can be very damaging to an asexual population, while leaving a sexual population virtually unscathed. Furthermore, in a changing environment, the advantages of sexuality over asexuality can be much greater than suggested by most previous studies. Our analysis applies in the case of very large populations, where stochastic forces may be neglected.     

The effect of mating system on invasiveness: some genetic load may be advantageous when invading new environments

The role of adaptation in determining invasion success has been acknowledged recently, notably through the accumulation of case studies of rapid evolution during bioinvasions. Despite this growing body of empirical evidence, there is still a need to develop the theoretical background of invasions with adaptation. Specifically, the impact of mating system on the dynamics of adaptation during invasion of a new environment remains only partially understood. Here, we analyze a simulation demo-genetic model of bioinvasion accounting for partial asexuality rates. We simulate two levels of recurrent immigration from a source population at mutation–drift–selection equilibrium to a new empty environment with a different adaptive landscape (black-hole sink). Adaptation relies on a quantitative trait coded explicitly by 10 loci under mutation, selection and genetic drift. Using this model, we confirm previous results on the positive effects on invasiveness of migration, mutation and similarity of local phenotypic optima. We further show how the invasion dynamics of the introduced population is affected by the rate of asexuality. Purely asexual species have lower invasion success in terms of probability and time to invasion than species with other mating systems. Among species with mixed mating systems, the greatest invasiveness is observed for species with high asexual rates. We suggest that this pattern is due to inflated genetic variance in the source population through the Hill-Robertson effect (i.e., clonal interference). An interesting consequence is that species with the highest genetic load in their source environment have greatest invasiveness in the new environment.     

Extreme genetic diversity in asexual grass thrips populations

The continuous generation of genetic variation has been proposed as one of the main factors explaining the maintenance of sexual reproduction in nature. However, populations of asexual individuals may attain high levels of genetic diversity through within‐lineage diversification, replicate transitions to asexuality from sexual ancestors and migration. How these mechanisms affect genetic variation in populations of closely related sexual and asexual taxa can therefore provide insights into the role of genetic diversity for the maintenance of sexual reproduction. Here, we evaluate patterns of intra‐ and interpopulation genetic diversity in sexual and asexual populations of Aptinothrips rufus grass thrips. Asexual A. rufus populations are found throughout the world, whereas sexual populations appear to be confined to few locations in the Mediterranean region. We found that asexual A. rufus populations are characterized by extremely high levels of genetic diversity, both in comparison with their sexual relatives and in comparison with other asexual species. Migration is extensive among asexual populations over large geographic distances, whereas close sexual populations are strongly isolated from each other. The combination of extensive migration with replicate evolution of asexual lineages, and a past demographic expansion in at least one of them, generated high local clone diversities in A. rufus. These high clone diversities in asexual populations may mimic certain benefits conferred by sex via genetic diversity and could help explain the extreme success of asexual A. rufus populations.     

Short-term population differences in the genetic architecture of life history traits related to sexuality in an aphid species

One of the most important factors that determine the evolutionary trajectory of a suite of traits in a population is the structure of the genetic variance-covariance matrix (G). We studied the cyclically parthenogenetic aphid Rhopalosiphum padi, whose populations exhibit two types of reproductive lineages respectively specialized in sexuality (that is, cyclically parthenogenetic lineages) and in asexuality (that is, obligate parthenogenetic lineages). We compared the quantitative genetics of life histories in these two lineage types. Our results suggest that both, the elements and the whole structure of the resulting G matrices differ in the very short term, between lineage types. This would involve the evolution toward different evolutionary optima in the same population, depending on whether sexual or asexual lineages predominate. Since sexual and asexual lineages vary seasonally in their abundance, a fluctuating selective regime has been proposed for this species, which would contribute to the maintenance of the reproductive polymorphism that these populations exhibit.     

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.     

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.     

LARGE POPULATION SIZE PREDICTS THE DISTRIBUTION OF ASEXUALITY IN SCALE INSECTS

Understanding why some organisms reproduce by sexual reproduction while others can reproduce asexually remains an important unsolved problem in evolutionary biology. Simple demography suggests that asexuals should outcompete sexually reproducing organisms, because of their higher intrinsic rate of increase. However, the majority of multicellular organisms have sexual reproduction. The widely accepted explanation for this apparent contradiction is that asexual lineages have a higher extinction rate. A number of models have indicated that population size might play a crucial role in the evolution of asexuality. The strength of processes that lead to extinction of asexual species is reduced when population sizes get very large, so that the long‐term advantage of sexual over asexual reproduction may become negligible. Here, we use a comparative approach using scale insects (Coccoidea, Hemiptera) to show that asexuality is indeed more common in species with larger population density and geographic distribution and we also show that asexual species tend to be more polyphagous. We discuss the implication of our findings for previously observed patterns of asexuality in agricultural pests.     

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.     

INBREEDING DEPRESSION UNDER JOINT SELFING,OUTCROSSING, AND ASEXUALITY

Partial asexual reproduction was introduced into a model of inbreeding depression due to nearly recessive lethal mutations in a partially selfing population. The frequencies of asexuality, selfing, and outcrossing were either constant or occurred in cycles of a single sexual generation followed by one or more asexual generations. We found that increasing the degree of asexuality generally increases the inbreeding depression maintained in an equilibrium population with a given selfing rate. This is due to the increase in the number of mutations relative to sexual generations during which selfing-induced purging of mutations may take place. For very high genomic mutation rates, sufficient to produce a threshold rate of self-fertilization for purging recessive lethal mutations, asexuality can have the opposite effect, decreasing equilibrium inbreeding depression, because of an increase in the efficiency of selection against mutations in heterozygotes with asexuality.     

The impact of interspecific competition on lineage evolution and a rapid peak shift by interdemic genetic mixing in experimental bacterial populations

Epistatic interactions between genes in the genome constrain the accessible evolutionary paths of lineages. Two factors involving epistasis that can affect the evolutionary path and fate of lineages were investigated. The first factor concerns the impact of competition with another species lineage that has different epistatic constraints. Five enteric bacterial populations were evolved by point mutation in medium containing a single limiting resource. Single-species and two-species cultures were used to determine whether different asexual lineages have different capacities for producing variants due to epistatic constraints, and whether their survival is determined by local inter-lineage competition with different species. Local inter-lineage competition quickly resulted in one successful lineage, with another lineage becoming extinct before finding a higher peak. The second factor concerns a peak-shifting process, and whether the sexual recombination between different demes can cause peak shifts was investigated. An Escherichia coli population consisting of a male (Hfr) and female strain (F(-)) was evolved in a single limiting resource and compared to evolving populations containing the male or female strain alone. The E. coli sexual lineage was successful due to its ability to escape lower peaks and reach a higher peak, not because of a rapid approach to the nearest local peak the male or female asexual lineage could reach. The data in this study demonstrate that lineage survivability can be determined by the ability to produce beneficial mutations and checked by local competition between lineages of different species. Interspecific competition may prevent a population from evolving through crossing fitness valleys or adaptive ridges if it requires many generations to achieve peak shifts. The data also show that genomic recombination between different conspecific lineages can rapidly carry the combined lineage to a higher peak.     

Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality,hybridization and speciation

Although sexual reproduction is ubiquitous throughout nature, the molecular machinery behind it has been repeatedly disrupted during evolution, leading to the emergence of asexual lineages in all eukaryotic phyla. Despite intensive research, little is known about what causes the switch from sexual reproduction to asexuality. Interspecific hybridization is one of the candidate explanations, but the reasons for the apparent association between hybridization and asexuality remain unclear. In this study, we combined cross‐breeding experiments with population genetic and phylogenomic approaches to reveal the history of speciation and asexuality evolution in European spined loaches (Cobitis). Contemporary species readily hybridize in hybrid zones, but produce infertile males and fertile but clonally reproducing females that cannot mediate introgressions. However, our analysis of exome data indicates that intensive gene flow between species has occurred in the past. Crossings among species with various genetic distances showed that, while distantly related species produced asexual females and sterile males, closely related species produce sexually reproducing hybrids of both sexes. Our results suggest that hybridization leads to sexual hybrids at the initial stages of speciation, but as the species diverge further, the gradual accumulation of reproductive incompatibilities between species could distort their gametogenesis towards asexuality. Interestingly, comparative analysis of published data revealed that hybrid asexuality generally evolves at lower genetic divergences than hybrid sterility or inviability. Given that hybrid asexuality effectively restricts gene flow, it may establish a primary reproductive barrier earlier during diversification than other “classical” forms of postzygotic incompatibilities. Hybrid asexuality may thus indirectly contribute to the speciation process.     

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.     

Clone mixtures and a pacemaker: new facets of Red-Queen theory and ecology

Host-parasite antagonistic interaction has been proposed as a potential agent to promote genetic polymorphism and to favour sex against asex, despite its twofold cost in reproduction. However, the host-parasite gene-for-gene dynamics often produce unstable cycles that tend to destroy genetic diversity. Here, we examine such diversity destroying coevolutionary dynamics of host and parasite, which is coupled through local or global migration, or both, between demes in a metapopulation structure. We show that, with global migration in the island model, peculiar out-of-phase islands spontaneously arise in the cluster of islands converging to a global synchrony. Such asynchrony induced by the 'pacemaker islands' serves to restore genetic variation. With increasing fraction of local migration, spots of asynchrony are converted into loci or foci of spiral and target patterns, whose rotating arms then cover the majority of demes. A multi-locus analogue of the model reproduces the same tendency toward asynchrony, and the condition arises for an advantage of asexual clones over their sexual counterpart when enough genetic diversity is maintained through metapopulation storage-migration serves as a cheap alternative to sex.     

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.     

The genetic outcomes of sex and recombination in long-term functionally parthenogenetic lineages of Australian Sitobion aphids

The typical life cycle of an aphid is cyclical parthenogenesis which involves the alternation of sexual and asexual reproduction. However, aphid life cycles, even within a species, can encompass everything on a continuum from obligate sexuality, through facultative sexuality to obligate asexuality. Loss of the sexual cycle in aphids is frequently associated with the introduction of a new pest and can occur for a number of environmental and genetic reasons. Here we investigate loss of sexual function in Sitobion aphids in Australia. Specifically, we aimed to determine whether an absence of sexual reproduction in Australian Sitobion results from genetic loss of sexual function or environmental constraints in the introduced range. We addressed our aims by performing a series of breeding experiments. We found that some lineages have genetically lost sexual function while others retain sexual function and appear environmentally constrained to asexuality. Further, in our crosses, using autosomal and X-linked microsatellite markers, we identified processes deviating from normal Mendelian segregation. We observed strong deviations in X chromosome transmission through the sexual cycle. Additionally, when progeny genotypes were examined across multiple loci simultaneously we found that some multilocus genotypes are significantly over-represented in the sample and that levels of heterozygosity were much higher than expected at almost all loci. This study demonstrates that strong biases in the transmission of X chromosomes through the sexual cycle are likely to be widespread in aphids. The mechanisms underlying these patterns are not clear. We discuss several possible alternatives, including mutation accumulation during periods of functional asexuality and genetic imprinting.     

Poor male function favours the coexistence of sexual and asexual relatives

Classical models of the evolution of sex typically assume that an asexual lineage, once derived, is reproductively separate from the sexual lineage from which it was derived. However, many asexuals, including hermaphrodite plants, produce male gametes capable of fertilising the eggs of co-existing sexuals, giving rise to sexual and asexual progeny. This male function of asexuals may be poor, and it has been proposed that this could favour sexuality and adversely affect the successful establishment of asexual lineages. We show that things are more complicated than this; the effect is frequency-dependent and poor male function may sometimes favour asexuality. In a spatially distributed population of flowering plants, it can prevent the successful invasion of either reproductive mode by the other via long-range dispersal. Consequently invasions must be driven by short-range dispersal, and are therefore extremely slow. Thus poor male function favours long-term co-existence of sexuals and asexuals. When coupled with the superior ability of asexuals to colonise virgin territory after an Ice Age, it may explain current ecological distribution patterns.     

Evolutionary history of contagious asexuality in Daphnia pulex

Asexual taxa are short-lived, suggesting that transitions to asexuality represent evolutionary dead-ends. However, with high rates of clonal origin and coexistence of asexuals and sexuals via selective asymmetries, asexuality may persist in the long term as a result of a dynamic equilibrium between clonal origin and extinction. Few such systems have been studied in detail. Here, we investigate the evolutionary history of asexual lineages of Daphnia pulex, which are derived from sexual relatives via the inheritance of a dominant female-limited meiosis-suppressing locus and inhabit ponds throughout northeastern North America (NA). Our extensive sampling and subsequent phylogenetic analysis using mitochondrial sequence data reveals a young and genetically diverse asexual assemblage, reflecting high rates of clonal origin due to the contagious nature of asexuality. Yet, asexuality is restricted to two phylogroups (B and C) with historical and/or present associations with northeastern NA and is absent from a northwestern phylogroup (A), supporting a recent northeastern origin of asexuality in this species. Furthermore, macrogeographic patterns of genetic variability indicate that phylogroups B and C recolonized northeastern NA from opposite directions, yet their presently overlapping geographic distributions are similarly divided into an eastern asexual and a western sexual region. We attribute these patterns to a recent contagious spread of asexuality from a northeastern source. If environment-mediated selective asymmetries play no significant role in determining the outcome of competitive interactions between sexuals and asexuals, regions of contact may be setting the stage for continued asexual conquests.