Solenn Stoeckel

Host range expansion of an introduced insect pest through multiple colonizations of specialized clones

Asexuality confers demographic advantages to invasive taxa, but generally limits adaptive potential for colonizing of new habitats. Therefore, pre‐existing adaptations and habitat tolerance are essential in the success of asexual invaders. We investigated these key factors of invasiveness by assessing reproductive modes and host‐plant adaptations in the pea aphid, Acyrthosiphon pisum, a pest recently introduced into Chile. The pea aphid encompasses lineages differing in their reproductive mode, ranging from obligatory cyclical parthenogenesis to fully asexual reproduction. This species also shows variation in host use, with distinct biotypes specialized on different species of legumes as well as more polyphagous populations. In central Chile, microsatellite genotyping of pea aphids sampled on five crops and wild legumes revealed three main clonal genotypes, which showed striking associations with particular host plants rather than sampling locations. Phenotypic analyses confirmed their strong host specialization and demonstrated parthenogenesis as their sole reproductive mode. The genetic relatedness of these clonal genotypes with corresponding host‐specialized populations from the Old World indicated that each clone descended from a particular Eurasian biotype, which involved at least three successful introduction events followed by spread on different crops. This study illustrates that multiple introductions of highly specialized clones, rather than local evolution in resource use and/or selection of generalist genotypes, can explain the demographic success of a strictly asexual invader.

Genome scans reveal candidate regions involved in the adaptation to host plant in the pea aphid complex

A major goal in evolutionary biology is to uncover the genetic basis of adaptation. Divergent selection exerted on ecological traits may result in adaptive population differentiation and reproductive isolation and affect differentially the level of genetic divergence along the genome. Genome‐wide scan of large sets of individuals from multiple populations is a powerful approach to identify loci or genomic regions under ecologically divergent selection. Here, we focused on the pea aphid, a species complex of divergent host races, to explore the organization of the genomic divergence associated with host plant adaptation and ecological speciation. We analysed 390 microsatellite markers located at variable distances from predicted genes in replicate samples of sympatric populations of the pea aphid collected on alfalfa, red clover and pea, which correspond to three common host‐adapted races reported in this species complex. Using a method that accounts for the hierarchical structure of our data set, we found a set of 11 outlier loci that show higher genetic differentiation between host races than expected under the null hypothesis of neutral evolution. Two of the outliers are close to olfactory receptor genes and three other nearby genes encoding salivary proteins. The remaining outliers are located in regions with genes of unknown functions, or which functions are unlikely to be involved in interactions with the host plant. This study reveals genetic signatures of divergent selection across the genome and provides an inventory of candidate genes responsible for plant specialization in the pea aphid, thereby setting the stage for future functional studies.

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.

Accelerated Evolution of Sex Chromosomes in Aphids, an X0 System

Sex chromosomes play a role in many important biological processes, including sex determination, genomic conflicts, imprinting, and speciation. In particular, they exhibit several unusual properties such as inheritance pattern, hemizygosity, and reduced recombination, which influence their response to evolutionary factors (e.g., drift, selection, and demography). Here, we examine the evolutionary forces driving X chromosome evolution in aphids, an XO system where females are homozygous (XX) and males are hemizygous (X0) at sex chromosomes. We show by simulations that the unusual mode of transmission of the X chromosome in aphids, coupled with cyclical parthenogenesis, results in similar effective population sizes and predicted levels of genetic diversity for X chromosomes and autosomes under neutral evolution. These results contrast with expectations from standard XX/XY or XX/X0 systems (where the effective population size of the X is three-fourths that of autosomes) and have deep consequences for aphid X chromosome evolution. We then localized 52 microsatellite markers on the X and 351 on autosomes. We genotyped 167 individuals with 356 of these loci and found similar levels of allelic richness on the X and on the autosomes, as predicted by our simulations. In contrast, we detected higher dN and dN/dS ratio for X-linked genes compared with autosomal genes, a pattern compatible with either positive or relaxed selection. Given that both types of chromosomes have similar effective population sizes and that the single copy of the X chromosome of male aphids exposes its recessive genes to selection, some degree of positive selection seems to best explain the higher rates of evolution of X-linked genes. Overall, this study highlights the particular relevance of aphids to study the evolutionary factors driving sex chromosomes and genome evolution.

RClone: a package to identify MultiLocus Clonal Lineages and handle clonal data sets in r.

Summary Partially, clonal species are common in the Tree of Life. And yet, population genetic models still mostly focus on the extremes: strictly sexual versus purely asexual reproduction. Here, we present an R package built upon genclone software including new functions and several improvements. The RClone package includes functions to handle clonal data sets, allowing (i) checking for data set reliability to discriminate multilocus genotypes (MLGs), (ii) ascertainment of MLG and semi-automatic determination of clonal lineages (MLL), (iii) genotypic richness and evenness indices calculation based on MLGs or MLLs and (iv) describing several spatial components of clonality. RClone allows the one-shot analysis of multipopulation data sets without size limitation, suitable for data sets now increasingly produced through next-generation sequencing. A major improvement compared to existing software is the ability to determine the threshold to cluster similar MLGs into MLLs, based on implemented simulations of sexual events. Several functions allow data importation, conversion and exportation with adegenet, Genetix or Arlequin. RClone is provided with two vignettes to handle analysis on one (RClone_quickmanual) or several populations (RClone_qmsevpops).

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 FIS 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.

Genetic diversity and fitness in small populations of partially asexual, self-incompatible plants.

How self-incompatibility systems are maintained in plant populations is still a debated issue. Theoretical models predict that self-incompatibility systems break down according to the intensity of inbreeding depression and number of S-alleles. Other studies have explored the function of asexual reproduction in the maintenance of self-incompatibility. However, the population genetics of partially asexual, self-incompatible populations are poorly understood and previous studies have failed to consider all possible effects of asexual reproduction or could only speculate on those effects. In this study, we investigated how partial asexuality may affect genetic diversity at the S-locus and fitness in small self-incompatible populations. A genetic model including an S-locus and a viability locus was developed to perform forward simulations of the evolution of populations of various sizes. Drift combined with partial asexuality produced a decrease in the number of alleles at the S-locus. In addition, an excess of heterozygotes was present in the population, causing an increase in mutation load. This heterozygote excess was enhanced by the self-incompatibility system in small populations. In addition, in highly asexual populations, individuals produced asexually had some fitness advantages over individuals produced sexually, because sexual reproduction produces homozygotes of the deleterious allele, contrary to asexual reproduction. Our results suggest that future research on the function of asexuality for the maintenance of self-incompatibility will need to (1) account for whole-genome fitness (mutation load generated by asexuality, self-incompatibility and drift) and (2) acknowledge that the maintenance of self-incompatibility may not be independent of the maintenance of sex itself.

Parental participation in progeny and effective population sizes in experimental seed orchards of wild cherry Prunus avium L. (Batsch)

Parents and progenies genetic diversity, and male and female contributions to the seed crop were assessed in three experimental Prunus avium seed orchards. Collected data were used to compare different effective population sizes, based on phenological, seed crop and paternity analysis. Our results did not show any difference of genetic diversity between parents and progenies. A limited pollen pollution was detected. We showed that distance and coflowering among clones had a significant effect on effective pollination, and a significant effect of the production of flowers was revealed in one of the seed orchards. Our study also revealed a quite low number of effective size of fathers per mother, but high effective sizes of mothers, fathers and parents at the level of the seed orchard. Finally, the calculation of effective size of mothers, fathers and parents was not highly modified when having the complete information based on the paternity analysis.RésuméLa diversité génétique des parents et de leurs descendants, ainsi que les contributions mâle et femelle à la récolte de graines ont été estimées dans trois vergers à graines expérimentaux de Prunus avium. Les données collectées ont été utilisées pour comparer différentes tailles de population efficace, en se basant sur l’analyse de la phénologie, de la récolte de graines et de la paternité. Nos résultats n’ont pas montré de différence de diversité génétique entre les parents et les descendants. Une pollution pollinique limitée a été mise en évidence. Nous avons montré un effet significatif de la distance et de la cofloraison entre clones sur la pollinisation efficace, ainsi qu’un effet significatif de la production de fleurs dans l’un des vergers à graines. Notre étude a aussi révélé un faible nombre efficace de pères à l’échelle de chaque mère, et un nombre efficace de mères, de pères et de parents important à l’échelle du verger à graines. Enfin, le calcul des tailles efficaces de pères et de parents à l’échelle du verger à graines n’a pas été fortement influencé par le fait d’avoir l’information totale de contribution donnée par l’analyse de paternité.

Polymorphism pattern at a miniature inverted-repeat transposable element locus downstream of the domestication gene Teosinte-branched1 in wild and domesticated pearl millet

Unravelling the mechanisms involved in adaptation to understand plant morphological evolution is a challenging goal. For crop species, identification of molecular causal polymorphisms involved in domestication traits is central to this issue. Pearl millet, a domesticated grass mostly found in semi‐arid areas of Africa and India, is an interesting model to address this topic: the domesticated form shares common derived phenotypes with some other cereals such as a decreased ability to develop basal and axillary branches in comparison with the wild phenotype. Two recent studies have shown that the orthologue of the maize gene Teosinte‐Branched1 in pearl millet (PgTb1) was probably involved in branching evolution during domestication and that a miniature inverted‐repeat transposable element (MITE) of the Tuareg family was inserted in the 3′ untranslated region of PgTb1. For a set of 35 wild and domesticated populations, we compared the polymorphism patterns at this MITE and at microsatellite loci. The Tuareg insertion was nearly absent in the wild populations, whereas a strong longitudinal frequency cline was observed in the domesticated populations. The geographical pattern revealed by neutral microsatellite loci clearly demonstrated that isolation by distance does not account for the existence of this cline. However, comparison of population differentiation at the microsatellite and the MITE loci and analyses of the nucleotide polymorphism pattern in the downstream region of PgTb1 did not show evidence that the cline at the MITE locus has been shaped by selection, suggesting the implication of a neutral process. Alternative hypotheses are discussed.