GenAPoPop 1.0: A user-friendly software to analyse genetic diversity and structure from partially clonal and selfed autopolyploid organisms.

Autopolyploidy is quite common in most clades of eukaryotes. The emergence of sequence-based genotyping methods with individual and marker tags now enables confident allele dosage, overcoming the main obstacle to the democratization of the population genetic approaches when studying ecology and evolution of autopolyploid populations and species. Reproductive modes, including clonality, selfing and allogamy, have deep consequences on the ecology and evolution of population and species. Analysing genetic diversity and its dynamics over generations is one efficient way to infer the relative importance of clonality, selfing and allogamy in populations. GenAPoPop is a user-friendly solution to compute the specific corpus of population genetic indices, including indices about genotypic diversity, needed to analyse partially clonal, selfed and allogamous polysomic populations genotyped with confident allele dosage. It also easily provides the posterior probabilities of quantitative reproductive modes in autopolyploid populations genotyped at two-time steps and a graphical representation of the minimum spanning trees of the genetic distances between polyploid individuals, facilitating the interpretation of the genetic coancestry between individuals in hierarchically structured populations. GenAPoPop complements the previously existing solutions, including SPAGEDI and POLYGENE, to use genotypings to study the ecology and evolution of autopolyploid populations. It was specially developed with a simple graphical interface and workflow, and comes with a simulator to facilitate practical courses and teaching of population genetics for autopolyploid populations.

Approximate Bayesian Computation applied to time series of population genetic data disentangles rapid genetic changes and demographic variations in a pathogen population.

Adaptation can occur at remarkably short timescales in natural populations, leading to drastic changes in phenotypes and genotype frequencies over a few generations only. The inference of demographic parameters can allow understanding how evolutionary forces interact and shape the genetic trajectories of populations during rapid adaptation. Here we propose a new Approximate Bayesian Computation (ABC) framework that couples a forward and individual-based model with temporal genetic data to disentangle genetic changes and demographic variations in a case of rapid adaptation. We test the accuracy of our inferential framework and evaluate the benefit of considering a dense versus sparse sampling. Theoretical investigations demonstrate high accuracy in both model and parameter estimations, even if a strong thinning is applied to time series data. Then, we apply our ABC inferential framework to empirical data describing the population genetic changes of the poplar rust pathogen following a major event of resistance overcoming. We successfully estimate key demographic and genetic parameters, including the proportion of resistant hosts deployed in the landscape and the level of standing genetic variation from which selection occurred. Inferred values are in accordance with our empirical knowledge of this biological system. This new inferential framework, which contrasts with coalescent-based ABC analyses, is promising for a better understanding of evolutionary trajectories of populations subjected to rapid adaptation.

Tetrasporophytic bias coupled with heterozygote deficiency in Antarctic Plocamium sp. (Florideophyceae, Rhodophyta).

Meiosis and syngamy generate an alternation between two ploidy stages, but the timing of these two processes varies widely across taxa, thereby generating life cycle diversity. One hypothesis suggests that life cycles with long-lived haploid stages are correlated with selfing, asexual reproduction, or both. Though mostly studied in angiosperms, selfing and asexual reproduction are often associated with marginal habitats. Yet, in haploid-diploid macroalgae, these two reproductive modes have subtle but unique consequences whereby predictions from angiosperms may not apply. Along the western Antarctic Peninsula, there is a thriving macroalgal community, providing an opportunity to explore reproductive system variation in haploid-diploid macroalgae at high latitudes where endemism is common. Plocamium sp. is a widespread and abundant red macroalga observed within this ecosystem. We sampled 12 sites during the 2017 and 2018 field seasons and used 10 microsatellite loci to describe the reproductive system. Overall genotypic richness and evenness were high, suggesting sexual reproduction. Eight sites were dominated by tetrasporophytes, but there was strong heterozygote deficiency, suggesting intergametophytic selfing. We observed slight differences in the prevailing reproductive mode among sites, possibly due to local conditions (e.g., disturbance) that may contribute to site-specific variation. It remains to be determined whether high levels of selfing are characteristic of macroalgae more generally at high latitudes, due to the haploid-diploid life cycle, or both. Further investigations of algal life cycles will likely reveal the processes underlying the maintenance of sexual reproduction more broadly across eukaryotes, but more studies of natural populations are required.

Improving sustainable crop protection using population genetics concepts.

Growing genetically resistant plants allows pathogen populations to be controlled and reduces the use of pesticides. However, pathogens can quickly overcome such resistance. In this context, how can we achieve sustainable crop protection? This crucial question has remained largely unanswered despite decades of intense debate and research effort. In this study, we used a bibliographic analysis to show that the research field of resistance durability has evolved into three subfields: (1) "plant breeding" (generating new genetic material), (2) "molecular interactions" (exploring the molecular dialogue governing plant-pathogen interactions) and (3) "epidemiology and evolution" (explaining and forecasting of pathogen population dynamics resulting from selection pressure[s] exerted by resistant plants). We argue that this triple split of the field impedes integrated research progress and ultimately compromises the sustainable management of genetic resistance. After identifying a gap among the three subfields, we argue that the theoretical framework of population genetics could bridge this gap. Indeed, population genetics formally explains the evolution of all heritable traits, and allows genetic changes to be tracked along with variation in population dynamics. This provides an integrated view of pathogen adaptation, in particular via evolutionary-epidemiological feedbacks. In this Opinion Note, we detail examples illustrating how such a framework can better inform best practices for developing and managing genetically resistant cultivars.

The advantage of sex: Reinserting fluctuating selection in the pluralist approach.

The advantage of sex, and its fixation in some clades and species all over the eukaryote tree of life, is considered an evolutionary enigma, especially regarding its assumed two-fold cost. Several likely hypotheses have been proposed such as (1) a better response to the negative frequency-dependent selection imposed by the "Red Queen" hypothesis; (2) the competition between siblings induced by the Tangled Bank hypothesis; (3) the existence of genetic and of (4) ecological factors that can diminish the cost of sex to less than the standard assumed two-fold; and (5) a better maintenance of genetic diversity and its resulting phenotypic variation, providing a selective advantage in randomly fluctuating environments. While these hypotheses have mostly been studied separately, they can also act simultaneously. This was advocated by several studies which presented a pluralist point of view. Only three among the five causes cited above were considered yet in such a framework: the Red Queen hypothesis, the Tangled Bank and the genetic factors lowering the cost of sex. We thus simulated the evolution of a finite mutating population undergoing negative frequency-dependent selection on phenotypes and a two-fold (or less) cost of sexuality, experiencing randomly fluctuating selection along generations. The individuals inherited their reproductive modes, either clonal or sexual. We found that exclusive sexuality begins to fix in populations exposed to environmental variation that exceeds the width of one ecological niche (twice the standard deviation of a Gaussian response to environment). This threshold was lowered by increasing negative frequency-dependent selection and when reducing the two-fold cost of sex. It contributes advocating that the different processes involved in a short-term advantage of sex and recombination can act in combination to favor the fixation of sexual reproduction in populations.

The Combined Effect of Haplodiplonty and Partial Clonality on Genotypic and Genetic Diversity in a Finite Mutating Population.

Partial clonality is known to affect the genetic composition and evolutionary trajectory of diplontic (single, free-living diploid stage) populations. However, many partially clonal eukaryotes exhibit life cycles in which somatic development occurs in both haploid and diploid individuals (haplodiplontic life cycles). Here, we studied how haplodiplontic life cycles and partial clonality structurally constrain, as immutable parameters, the reshuffling of genetic diversity and its dynamics in populations over generations. We assessed the distribution of common population genetic indices at different proportions of haploids, rates of clonality, mutation rates, and sampling efforts. Our results showed that haplodiplontic life cycles alone in finite populations affect effective population sizes and the ranges of distributions of population genetic indices. With nonoverlapping generations, haplodiplonty allowed the evolution of 2 temporal genetic pools that may diverge in sympatry due to genetic drift under full sexuality and clonality. Partial clonality in these life cycles acted as a homogenizing force between those 2 pools. Moreover, the combined effects of proportion of haploids, rate of clonality, and the relative strength of mutation versus genetic drift impacts the distributions of population genetics indices, rendering it difficult to transpose and use knowledge accumulated from diplontic or haplontic species. Finally, we conclude by providing recommendations for sampling and analyzing the population genetics of partially clonal haplodiplontic taxa.

Untangling structural factors driving genome stabilization in nascent Brassica napus allopolyploids.

Allopolyploids have globally higher fitness than their diploid progenitors; however, by comparison, most resynthesized allopolyploids have poor fertility and highly unstable genome. Elucidating the evolutionary processes promoting genome stabilization and fertility is thus essential to comprehend allopolyploid success. Using the Brassica model, we mimicked the speciation process of a nascent allopolyploid species by resynthesizing allotetraploid Brassica napus and systematically selecting for euploid individuals over eight generations in four independent allopolyploidization events with contrasted genetic backgrounds, cytoplasmic donors, and polyploid formation type. We evaluated the evolution of meiotic behavior and fertility and identified rearrangements in S1 to S9 lineages to explore the positive consequences of euploid selection on B. napus genome stability. Recurrent selection of euploid plants for eight generations drastically reduced the percentage of aneuploid progenies as early as the fourth generation, concomitantly with a decrease in number of newly fixed homoeologous rearrangements. The consequences of homoeologous rearrangements on meiotic behavior and seed number depended strongly on the genetic background and cytoplasm donor. The combined use of both self-fertilization and recurrent euploid selection allowed identification of genomic regions associated with fertility and meiotic behavior, providing complementary evidence to explain B. napus speciation success.

The discernible and hidden effects of clonality on the genotypic and genetic states of populations: Improving our estimation of clonal rates.

Partial clonality is widespread across the tree of life, but most population genetic models are designed for exclusively clonal or sexual organisms. This gap hampers our understanding of the influence of clonality on evolutionary trajectories and the interpretation of population genetic data. We performed forward simulations of diploid populations at increasing rates of clonality (c), analysed their relationships with genotypic (clonal richness, R, and distribution of clonal sizes, Pareto ß) and genetic (FIS and linkage disequilibrium) indices, and tested predictions of c from population genetic data through supervised machine learning. Two complementary behaviours emerged from the probability distributions of genotypic and genetic indices with increasing c. While the impact of c on R and Pareto ß was easily described by simple mathematical equations, its effects on genetic indices were noticeable only at the highest levels (c > 0.95). Consequently, genotypic indices allowed reliable estimates of c, while genetic descriptors led to poorer performances when c < 0.95. These results provide clear baseline expectations for genotypic and genetic diversity and dynamics under partial clonality. Worryingly, however, the use of realistic sample sizes to acquire empirical data systematically led to gross underestimates (often of one to two orders of magnitude) of c, suggesting that many interpretations hitherto proposed in the literature, mostly based on genotypic richness, should be reappraised. We propose future avenues to derive realistic confidence intervals for c and show that, although still approximate, a supervised learning method would greatly improve the estimation of c from population genetic data.

Exploring the Genetic Consequences of Clonality in Haplodiplontic Taxa.

Partially clonality is an incredibly common reproductive mode found across all the major eukaryotic lineages. Yet, population genetic theory is based on exclusive sexuality or exclusive asexuality, and partial clonality is often ignored. This is particularly true in haplodiplontic eukaryotes, including algae, ferns, mosses, and fungi, where somatic development occurs in both the haploid and diploid stages. Haplodiplontic life cycles are predicted to be correlated with asexuality, but tests of this prediction are rare. Moreover, there are unique consequences of having long-lived haploid and diploid stages in the same life cycle. For example, clonal processes uncouple the life cycle such that the repetition of the diploid stage via clonality leads to the loss of the haploid stage. Here, we surveyed the literature to find studies that had genotyped both haploid and diploid stages and recalculated population genetic summary metrics for seven red algae, one green alga, three brown algae, and three mosses. We compared these data to recent simulations that explicitly addressed the population genetic consequences of partial clonality in haplodiplontic life cycles. Not only was partial clonality found to act as a homogenizing force, but the combined effects of proportion of haploids, rate of clonality, and the relative strength of mutation versus genetic drift impacts the distributions of population genetic indices. We found remarkably similar patterns across commonly used population genetic metrics between our empirical and recent theoretical expectations. To facilitate future studies, we provide some recommendations for sampling and analyzing population genetic parameters for haplodiplontic taxa.

Self-incompatibility limits sexual reproduction rather than environmental conditions in an invasive water primrose.

Fruit-set and seed-set depend on environmental conditions and reproductive systems. They are important components of sexual reproductive success in plants. They also control the ecological success and adaptation of invasive plants within their non-native ecosystems. We studied which factors bring about fruit-set and seed-set in invasive populations of the aquatic plant Ludwigia grandiflora subsp. hexapetala. We analyzed fruit set and seed set in 37 populations growing under variable climatic conditions in Western Europe. Sub-samples of seven fruitful and fruitless populations were grown in common controlled conditions. We carried out self- and cross-pollinations, and measured the floral morphometry. Environmental conditions did not affect fruit-set and seed-set in-situ and in common controlled environments. Hand-pollinations showed that individuals from fruitful populations exhibited fruit and seed production whatever the pollen donor, whereas individuals from fruitless populations only did so when pollen came from fruitful populations. Floral morphometry evidenced the existence of two floral morphs that fully overlapped with fruitfulness, and individual incompatibility. Our results rebutted the hypothesis that environmental variations control fruit set and seed set in these invasive populations. We instead showed that fruit set and seed set were controlled by a heteromorphic reproductive system involving a self-incompatible and inter-morph compatible morph (long-styled morph), and a self- and inter-morph compatible reverse morph (short-styled morph). We collected morphs and fruit set records of this species worldwide and found the same relationship: fruitless populations were all composed only of individuals with long-styled floral morph. Our study constitutes the first evidence of a heteromorphic self-incompatible system in Ludwigia genus and Onagraceae family.

After a catastrophe, a little bit of sex is better than nothing: Genetic consequences of a major earthquake on asexual and sexual populations.

Catastrophic events can have profound effects on the demography of a population and consequently on genetic diversity. The dynamics of postcatastrophic recovery and the role of sexual versus asexual reproduction in buffering the effects of massive perturbations remain poorly understood, in part because the opportunity to document genetic diversity before and after such events is rare. Six natural (purely sexual) and seven cultivated (mainly clonal due to farming practices) populations of the red alga Agarophyton chilense were surveyed along the Chilean coast before, in the days after and 2 years after the 8.8 magnitude earthquake in 2010. The genetic diversity of sexual populations appeared sensitive to this massive perturbation, notably through the loss of rare alleles immediately after the earthquake. By 2012, the levels of diversity returned to those observed before the catastrophe, probably due to migration. In contrast, enhanced rates of clonality in cultivated populations conferred a surprising ability to buffer the instantaneous loss of diversity. After the earthquake, farmers increased the already high rate of clonality to maintain the few surviving beds, but most of them collapsed rapidly. Contrasting fates between sexual and clonal populations suggest that betting on strict clonality to sustain production is risky, probably because this extreme strategy hampered adaptation to the brutal environmental perturbation induced by the catastrophe.

New insights into the population genetics of partially clonal organisms: When seagrass data meet theoretical expectations.

Seagrass meadows are among the most important coastal ecosystems in terms of both spatial extent and ecosystem services, but they are also declining worldwide. Understanding the drivers of seagrass meadow dynamics is essential for designing sound management, conservation and restoration strategies. However, poor knowledge of the effect of clonality on the population genetics of natural populations severely limits our understanding of the dynamics and connectivity of meadows. Recent modelling approaches have described the expected distributions of genotypic and genetic descriptors under increasing clonal rates, which may help us better understand and interpret population genetics data obtained for partial asexuals. Here, in the light of these recent theoretical developments, we revisited population genetics data for 165 meadows of four seagrass species. Contrasting shoot lifespan and rhizome turnover led to the prediction that the influence of asexual reproduction would increase along a gradient from Zostera noltii to Zostera marina, Cymodocea nodosa and Posidonia oceanica, with increasing departure from Hardy-Weinberg equilibrium (Fis ), mostly towards heterozygote excess, and decreasing genotypic richness (R). This meta-analysis provides a nested validation of this hypothesis at both the species and meadow scales through a significant relationship between Fis and R within each species. By empirically demonstrating the theoretical expectations derived from recent modelling approaches, this work calls for the use of Hardy-Weinberg equilibrium (Fis ) rather than only the strongly sampling-sensitive R to assess the importance of clonal reproduction (c), at least when the impact of selfing on Fis can be neglected. The results also emphasize the need to revise our appraisal of the extent of clonality and its influence on the dynamics, connectivity and evolutionary trajectory of partial asexuals in general, including in seagrass meadows, to develop the most accurate management strategies.

Hypomethylation of the aquatic invasive plant, Ludwigia grandiflora subsp. hexapetala mimics the adaptive transition into the terrestrial morphotype.

Ongoing global changes affect ecosystems and open up new opportunities for biological invasion. The ability of invasive species to rapidly adapt to new environments represents a relevant model for studying short-term adaptation mechanisms. The aquatic invasive plant, Ludwigia grandiflora subsp. hexapetala, is classified as harmful in European rivers. In French wet meadows, this species has shown a rapid transition from aquatic to terrestrial environments with emergence of two distinct morphotypes in 5 years. To understand the heritable mechanisms involved in adjustment to such a new environment, we investigate both genetic and epigenetic as possible sources of flexibility involved in this fast terrestrial transition. We found a low overall genetic differentiation between the two morphotypes arguing against the possibility that terrestrial morphotype emerged from a new adaptive genetic capacity. Artificial hypomethylation was induced on both morphotypes to assess the epigenetic hypothesis. We analyzed global DNA methylation, morphological changes, phytohormones and metabolite profiles of both morphotype responses in both aquatic and terrestrial conditions in shoot and root tissues. Hypomethylation significantly affected morphological variables, phytohormone levels and the amount of some metabolites. The effects of hypomethylation depended on morphotypes, conditions and plant tissues, which highlighted differences among the morphotypes and their plasticity. Using a correlative integrative approach, we showed that hypomethylation of the aquatic morphotype mimicked the characteristics of the terrestrial morphotype. Our data suggest that DNA methylation rather than a new adaptive genetic capacity is playing a key role in L. grandiflora subsp. hexapetala plasticity during its rapid aquatic to terrestrial transition.

ClonEstiMate, a Bayesian method for quantifying rates of clonality of populations genotyped at two-time steps.

Partial clonality is commonly used in eukaryotes and has large consequences for their evolution and ecology. Assessing accurately the relative importance of clonal vs. sexual reproduction matters for studying and managing such species. Here, we proposed a Bayesian approach, ClonEstiMate, to infer rates of clonality c from populations sampled twice over a short time interval, ideally one generation time. The method relies on the likelihood of the transitions between genotype frequencies of ancestral and descendent populations, using an extended Wright-Fisher model explicitly integrating reproductive modes. Our model provides posterior probability distribution of inferred c, given the assumed rates of mutation, as well as inbreeding and selfing when occurring. Tested under various conditions, this model provided accurate inferences of c, especially when the amount of information was modest, that is low sample sizes, few loci, low polymorphism and strong linkage disequilibrium. Inferences remained robust when mutation models and rates were misinformed. However, the method was sensitive to moderate frequencies of null alleles and when the time interval between required samplings exceeding two generations. Misinformed rates on mating modes (inbreeding and selfing) also resulted in biased inferences. Our method was tested on eleven data sets covering five partially clonal species, for which the extent of clonality was formerly deciphered. It delivered highly consistent results with previous information on the biology of those species. ClonEstiMate represents a powerful tool for detecting and inferring clonality in finite populations, genotyped with SNPs or microsatellites. It is freely available at https://www6.rennes.inra.fr/igepp_eng/Productions/Software.

Hybridization between two cryptic filamentous brown seaweeds along the shore: analysing pre- and postzygotic barriers in populations of individuals with varying ploidy levels.

We aimed to study the importance of hybridization between two cryptic species of the genus Ectocarpus, a group of filamentous algae with haploid-diploid life cycles that include the principal genetic model organism for the brown algae. In haploid-diploid species, the genetic structure of the two phases of the life cycle can be analysed separately in natural populations. Such life cycles provide a unique opportunity to estimate the frequency of hybrid genotypes in diploid sporophytes and meiotic recombinant genotypes in haploid gametophytes allowing the effects of reproductive barriers preventing fertilization or preventing meiosis to be untangle. The level of hybridization between E. siliculosus and E. crouaniorum was quantified along the European coast. Clonal cultures (568 diploid, 336 haploid) isolated from field samples were genotyped using cytoplasmic and nuclear markers to estimate the frequency of hybrid genotypes in diploids and recombinant haploids. We identified admixed individuals using microsatellite loci, classical assignment methods and a newly developed Bayesian method (XPloidAssignment), which allows the analysis of populations that exhibit variations in ploidy level. Over all populations, the level of hybridization was estimated at 8.7%. Hybrids were exclusively observed in sympatric populations. More than 98% of hybrids were diploids (40% of which showed signs of aneuploidy) with a high frequency of rare alleles. The near absence of haploid recombinant hybrids demonstrates that the reproductive barriers are mostly postzygotic and suggests that abnormal chromosome segregation during meiosis following hybridization of species with different genome sizes could be a major cause of interspecific incompatibility in this system.

Rare sex or out of reach equilibrium? The dynamics of F IS in partially clonal organisms.

BACKGROUND: Partially clonal organisms are very common in nature, yet the influence of partial asexuality on the temporal dynamics of genetic diversity remains poorly understood. Mathematical models accounting for clonality predict deviations only for extremely rare sex and only towards mean inbreeding coefficient [Formula: see text]. Yet in partially clonal species, both F IS < 0 and F IS > 0 are frequently observed also in populations where there is evidence for a significant amount of sexual reproduction. Here, we studied the joint effects of partial clonality, mutation and genetic drift with a state-and-time discrete Markov chain model to describe the dynamics of F IS over time under increasing rates of clonality. RESULTS: Results of the mathematical model and simulations show that partial clonality slows down the asymptotic convergence to F IS = 0. Thus, although clonality alone does not lead to departures from Hardy-Weinberg expectations once reached the final equilibrium state, both negative and positive F IS values can arise transiently even at intermediate rates of clonality. More importantly, such "transient" departures from Hardy Weinberg proportions may last long as clonality tunes up the temporal variation of F IS and reduces its rate of change over time, leading to a hyperbolic increase of the maximal time needed to reach the final mean [Formula: see text] value expected at equilibrium. CONCLUSION: Our results argue for a dynamical interpretation of F IS in clonal populations. Negative values cannot be interpreted as unequivocal evidence for extremely scarce sex but also as intermediate rates of clonality in finite populations. Complementary observations (e.g. frequency distribution of multiloci genotypes, population history) or time series data may help to discriminate between different possible conclusions on the extent of clonality when mean [Formula: see text] values deviating from zero and/or a large variation of F IS over loci are observed.

Interpretation and approximation tools for big, dense Markov chain transition matrices in population genetics.

BACKGROUND: Markov chains are a common framework for individual-based state and time discrete models in evolution. Though they played an important role in the development of basic population genetic theory, the analysis of more complex evolutionary scenarios typically involves approximation with other types of models. As the number of states increases, the big, dense transition matrices involved become increasingly unwieldy. However, advances in computational technology continue to reduce the challenges of "big data", thus giving new potential to state-rich Markov chains in theoretical population genetics. RESULTS: Using a population genetic model based on genotype frequencies as an example, we propose a set of methods to assist in the computation and interpretation of big, dense Markov chain transition matrices. With the help of network analysis, we demonstrate how they can be transformed into clear and easily interpretable graphs, providing a new perspective even on the classic case of a randomly mating, finite population with mutation. Moreover, we describe an algorithm to save computer memory by substituting the original matrix with a sparse approximate while preserving its mathematically important properties, including a closely corresponding dominant (normalized) eigenvector. A global sensitivity analysis of the approximation results in our example shows that size reduction of more than 90 % is possible without significantly affecting the basic model results. Sample implementations of our methods are collected in the Python module mamoth. CONCLUSION: Our methods help to make stochastic population genetic models involving big, dense transition matrices computationally feasible. Our visualization techniques provide new ways to explore such models and concisely present the results. Thus, our methods will contribute to establish state-rich Markov chains as a valuable supplement to the diversity of population genetic models currently employed, providing interesting new details about evolution e.g. under non-standard reproductive systems such as partial clonality.

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.

The exact distributions of F(IS) under partial asexuality in small finite populations with mutation.

Reproductive systems like partial asexuality participate to shape the evolution of genetic diversity within populations, which is often quantified by the inbreeding coefficient F IS. Understanding how those mating systems impact the possible distributions of F IS values in theoretical populations helps to unravel forces shaping the evolution of real populations. We proposed a population genetics model based on genotypic states in a finite population with mutation. For populations with less than 400 individuals, we assessed the impact of the rates of asexuality on the full exact distributions of F IS, the probabilities of positive and negative F IS, the probabilities of fixation and the probabilities to observe changes in the sign of F IS over one generation. After an infinite number of generations, we distinguished three main patterns of effects of the rates of asexuality on genetic diversity that also varied according to the interactions of mutation and genetic drift. Even rare asexual events in mainly sexual populations impacted the balance between negative and positive F IS and the occurrence of extreme values. It also drastically modified the probability to change the sign of F IS value at one locus over one generation. When mutation prevailed over genetic drift, increasing rates of asexuality continuously increased the variance of F IS that reached its highest value in fully asexual populations. In consequence, even ancient asexual populations showed the entire F IS spectrum, including strong positive F IS. The prevalence of heterozygous loci only occurred in full asexual populations when genetic drift dominated.

Masculinization of the x chromosome in the pea aphid.

Evolutionary theory predicts that sexually antagonistic mutations accumulate differentially on the X chromosome and autosomes in species with an XY sex-determination system, with effects (masculinization or feminization of the X) depending on the dominance of mutations. Organisms with alternative modes of inheritance of sex chromosomes offer interesting opportunities for studying sexual conflicts and their resolution, because expectations for the preferred genomic location of sexually antagonistic alleles may differ from standard systems. Aphids display an XX/X0 system and combine an unusual inheritance of the X chromosome with the alternation of sexual and asexual reproduction. In this study, we first investigated theoretically the accumulation of sexually antagonistic mutations on the aphid X chromosome. Our results show that i) the X is always more favourable to the spread of male-beneficial alleles than autosomes, and should thus be enriched in sexually antagonistic alleles beneficial for males, ii) sexually antagonistic mutations beneficial for asexual females accumulate preferentially on autosomes, iii) in contrast to predictions for standard systems, these qualitative results are not affected by the dominance of mutations. Under the assumption that sex-biased gene expression evolves to solve conflicts raised by the spread of sexually antagonistic alleles, one expects that male-biased genes should be enriched on the X while asexual female-biased genes should be enriched on autosomes. Using gene expression data (RNA-Seq) in males, sexual females and asexual females of the pea aphid, we confirm these theoretical predictions. Although other mechanisms than the resolution of sexual antagonism may lead to sex-biased gene expression, we argue that they could hardly explain the observed difference between X and autosomes. On top of reporting a strong masculinization of the aphid X chromosome, our study highlights the relevance of organisms displaying an alternative mode of sex chromosome inheritance to understanding the forces shaping chromosome evolution.