A maternal gene mutation correlates with an ovary phenotype in a parthenogenetic wasp population.

Endoparasitoid wasps rely on maternal protein secretions, including viruses and virus-like particles (VLPs), to overcome host defense reactions. In the ichneumonid Venturia canescens, VLPs are assembled in the nuclei of ovarian calyx gland cells, secreted into the lumen of the gland, and eventually transmitted into the host caterpillar together with the parasitoid egg. One of the genes coding for VLP proteins, termed VLP1, exists in two alleles producing two structurally different proteins. Here we describe the establishment and initial phenotypic characterisation of two parthenogenetic laboratory strains, which differ in VLP1 as well as in other genetic markers. A comparison of calyx tissues from the two strains revealed morphological differences that seem to affect egg movement from the ovarioles into the oviduct. The observed histological changes are correlated with differences in egg maturation and embryonic development causing a delay in larval hatching in one of the strains. Under conditions that favour superparasitism, the two strains differ in the number of offspring produced.     

Detection of Gene Flow from Sexual to Asexual Lineages in Thrips tabaci (Thysanoptera: Thripidae)

Populations of Thrips tabaci are known to have two sympatric but genetically isolated reproductive modes, arrhenotoky (sexual reproduction) and thelytoky (asexual reproduction). Herein, we report behavioral, ecological and genetic studies to determine whether there is gene flow between arrhenotokous and thelytokous T. tabaci. We did not detect significant preference by arrhenotokous males to mate with females of a particular reproductive mode, nor did we detect significant behavioral differences between arrhenotokous males mated with arrhenotokous or thelytokous females in their pre-copulation, copulation duration and mating frequency. Productive gene transfer resulting from the mating between the two modes was experimentally confirmed. Gene transfer from arrhenotokous T. tabaci to thelytokous T. tabaci was further validated by confirmation of the passage of the arrhenotokous male-originated nuclear gene (histone H3 gene) allele to the F₂ generation. These behavioral, ecological and genetic studies confirmed gene transfer from the sexual arrhenotokous mode to the asexual thelytokous mode of T. tabaci in the laboratory. These results demonstrate that asexual T. tabaci populations may acquire genetic variability from sexual populations, which could offset the long-term disadvantage of asexual reproduction.     

Marginal distribution and high heterozygosity of asexual Caloglossa vieillardii (Delesseriaceae,Rhodophyta) along the Australian coasts

In animals and land plants, many asexual species originate through inter‐ or intraspecific crosses, and such heterozygous asexuals frequently are more abundant than their sexual relatives in marginal habitats. Although asexual species have been reported in various macroalgal taxa, detailed information regarding their distribution, heterozygosity, and origin is limited. Because many asexual tetrasporophyte strains of Caloglossa vieillardii have been isolated from South Australia, far from their core tropical habitats, we re‐examined the distribution range of asexual C. vieillardii and genotyped these and other western Pacific strains using an actin gene marker. We confirmed the marginal distribution of the asexuals; however, a small patch of sexual thalli was newly discovered 450 km further west from asexual populations in South Australia. Three heterozygous genotypes and one homozygous genotypes were detected from nine asexual populations; 21 heterozygous strains were obligately asexual, but one homozygous strain suddenly produced sexual gametophytes after several years of culture. We hypothesized that the most abundant heterozygous genotype (defined as type 3/4) in asexual populations occurred by a cross between type 3 and type 4 allele gametophytes, both of which were isolated from the Australian coasts. In the crossing experiments, certain combinations between type 3 females and type 4 males produced tetrasporophytes, which recycled successive tetrasporophytes. In the culture experiments, whereas both sexual and asexual strains successfully produced tetraspores at 12°C, no sexual strains released carpospores below 14°C. However, it is uncertain whether this slight difference of maturation temperature was related to the marginal distribution of asexual C. vieillardii.     

Mitochondrial DNA diversity and geographical distribution of sexual and asexual strains of the braconid parasitoid Meteorus pulchricornis

Asexuality is an important tool with regard to the use of parasitoid wasps as biocontrol agents. Asexual (apomictic thelytokous) strains of Meteorus pulchricornis (Wesmael) (Hymenoptera: Braconidae), a polyphagous endoparasitoid of lepidopteran larvae, are sympatric with sexual (arrhenotokous) strains in Japan. The results of phylogenetic analyses of mitochondrial cytochrome c oxidase subunit I (COI) sequences indicated two major haplotype groups on the Japanese islands. The northern group I predominantly contained sexual strains, whereas the southern group II contained both sexual and asexual strains. Most asexual strains were likely derived within group II. An asexual strain recently established in New Zealand has the identical haplotype to a strain in Japan and was proven to have originated from East Asia. Three hypotheses on the evolution of asexuality are discussed for this parasitoid wasp: recessive gene, hybridization, and cytoplasmic element.     

Two coexisting lines of the endoparasitoid Venturia canescens show differences in reproductive success under conspecific superparasitism

In a laboratory colony of the endoparasitic wasp Venturia canescens Grav. (Hymenoptera: Ichneumonidae), two genetically distinct lines (RP, RM) appear to coexist sympatrically. The two lines display pronounced differences in ovarian morphology, parasitism behaviour and number of offspring produced under competing superparasitism. Since V. canescens is a solitary endoparasitoid, larvae inside superparasitised hosts must compete for host possession. We examined the outcome of conspecific superparasitism between the wasp lines with different time intervals between ovipositions. The results showed that the competitive abilities of the two lines were not symmetrical. Further, the RM-line won a significantly higher fraction (around 60%) of the overall contests. Dissection of parasitoid larvae from their hosts indicated that most contests between competing larvae had occurred within the first 24 h of the eggs hatching, suggesting the advantage of the RM-line relates to physical combat. It was previously thought that the coexistence of the two lines was exclusively due to maternal effects. The results of this study indicate for the first time that these differences are based on phenotypic variations in both the larval offspring and the mother.     

Does a deletion in a virus-like particle protein have pleiotropic effects on the reproductive biology of a parasitoid wasp?

Endoparasitoid insects have evolved mechanisms to counteract host immune defences. At oviposition, the endoparasitoid Venturia canescens injects virus-like particles (VLPs) together with the egg that interfere with the immune system of the host. These prevent encapsulation of the parasitoid egg. It has been shown that the gene coding for one of the VLP proteins exists in two variants (called Repeat-Plus (RP) and Repeat-Minus (RM)). Previous observations suggested that these variants induce pleiotropic effects on the reproductive biology of the female resulting, in an impeded transfer of eggs from the ovarioles to the oviducts in RM females, and in alterations in the egg laying sequence. We show that RM females from another geographical locality do not exhibit any phenotypic alteration of the reproductive biology. By showing a lack of association between VLP alleles and the reproductive phenotypic characteristics in a given strain, our results do not support the hypothesis of pleiotropic effects. Conversely, the results suggest that different genes code for the VLPs and for the reproductive biology characteristics. Different phenomena such as linkage, the action of pathogens, etc. could explain the association between characters that is observed in some strains.     

Genetic variability of arrhenotokous and thelytokous Venturia canescens (Hymenoptera)

The ichneumonid wasp Venturia canescens (Hymenoptera) has been studied extensively for foraging behaviour and population dynamics of sexually (arrhenotokous) and parthenogenetically (thelytokous) reproducing individuals. Here we report the development of a set of microsatellite markers for V.canescens and use them to show that arrhenotokous individuals have more genetic variability than thelytokous ones, which are even homozygous for all tested loci. Crosses between arrhenotokous individuals suggested one marker, Vcan071, to be linked with the Complementary Sex Determiner (CSD) locus and one, Vcan109, with the Virus Like Protein (vlp-p40) locus. The genome size of V. canescens was estimated to be 274-279?Mb. We discuss how both reproductive modes can give rise to the observed genetic variability and how the new markers can be used for future genetic studies of V. canescens.     

Gene flow between arrhenotokous and thelytokous populations of Venturia canescens (Hymenoptera)

In the solitary parasitoid wasp Venturia canescens both arrhenotokously (sexual) and thelytokously (parthenogenetical) reproducing individuals occur sympatrically. We found in the laboratory that thelytokous wasps are able to mate, receive and use sperm of arrhenotokous males. Using nuclear (amplified fragment length polymorphism, virus-like protein) and mitochondrial (restriction fragment length polymorphism) markers, we show the occurrence of gene flow from the arrhenotokous to the thelytokous mode in the field. Our results reinforce the paradox of sex in this species.     

A population of sexual Daphnia pulex resists invasion by asexual clones

Asexual reproduction avoids the costs associated with sex, predicting that invading asexual clones can quickly replace sexual populations. Daphnia pulex populations in the Great Lakes area are predominately asexual, but the elimination of sexual populations by invading clones is poorly understood. Asexual clones were detected at low frequency in one rare sexual population in 1995, with some increase in frequency during 2003 and 2004. However, these clones remained at low frequency during further yearly sampling (2005–2013) with no evidence that the resident sexual population was in danger of elimination. There was evidence for hybridization between rare males produced by asexual clones and sexual females with the potential to produce new asexual genotypes and spread the genetic factors for asexuality. In a short-term laboratory competition experiment, the two most common asexual clones did not increase in frequency relative to a genetically diverse sexual population due in part to a greater investment in diapausing eggs that trades-off current population growth for increased contribution to the egg bank. Our results suggest that a successful invasion can be prolonged, requiring a combination of clonal genotypes with high fitness, persistence of clones in the egg bank and negative factors affecting the sexual population such as inbreeding depression resulting from population bottlenecks.     

Gene flow between sexual and asexual strains of parasitic wasps: a possible case of sympatric speciation caused by a parthenogenesis-inducing bacterium

Sympatric speciation is strictly defined as the emergence of two species from a population in which mating has been random with respect to the place of birth of the mating partners. Mathematical models have shown that sympatric speciation is possible, but very few examples have been documented in nature. In this article, we demonstrate that arrhenotokous and thelytokous strains of a parasitic wasp, Neochrysocharis formosa, speciated sympatrically through infection by a symbiotic bacterium Rickettsia for the following reasons: First, Rickettsia infection was detected in all of the thelytokous strains collected throughout Japan. Second, the arrhenotokous and thelytokous strains have been collected sympatrically. Third, crossing experiments between the two strains did not result in fertilized offspring. In addition, the two strains were genetically isolated at the nuclear and mitochondrial genes. Fourth, the two strains showed a sister relationship in nuclear 28S rRNA gene. Finally, thelytokous females treated with antibiotics produced Rickettsia-free male offspring of the same reproductive form as arrhenotokous females indicating that the thelytokous strain could have speciated sympatrically from an individual of the arrhenotokous strain.     

Geographical distribution and genetic relatedness of sympatrical thelytokous and arrhenotokous populations of the parasitoid Venturia canescens (Hymenoptera)

Theory predicts that asexual reproduction has a competitive advantage over sexual reproduction because of the twofold cost of producing males. Few systems are suitable for directly testing this prediction. In the solitary parasitoid wasp Venturia canescens both arrhenotokously (sexual) and thelytokously (asexual) reproducing individuals occur sympatrically. We sampled 922 wasps from 22 localities along the coast of south‐eastern France. Thelytokous wasps were less abundant (23%) than arrhenotokous wasps and were almost always found in sympatry with arrhenotokous ones. An analysis of genetic relatedness using amplified fragment length polymorphism (AFLP) markers showed the existence of a widespread thelytokous clone. In addition, a few thelytokous individuals were found to be closely related to arrhenotokous ones and vice versa. These data suggest the occurrence of occasional gene flow between both reproductive modes and/or recurrent origin of thelytokous clones from coexisting arrhenotokous populations in the area. The results are discussed in the context of the paradox of sex.     

Genetic variation and asexual reproduction in the facultatively parthenogenetic cockroach Nauphoeta cinerea: implications for the evolution of sex

Asexual reproduction could offer up to a two‐fold fitness advantage over sexual reproduction, yet higher organisms usually reproduce sexually. Even in facultatively parthenogenetic species, where both sexual and asexual reproduction is sometimes possible, asexual reproduction is rare. Thus, the debate over the evolution of sex has focused on ecological and mutation‐elimination advantages of sex. An alternative explanation for the predominance of sex is that it is difficult for an organism to accomplish asexual reproduction once sexual reproduction has evolved. Difficulty in returning to asexuality could reflect developmental or genetic constraints. Here, we investigate the role of genetic factors in limiting asexual reproduction in Nauphoeta cinerea, an African cockroach with facultative parthenogenesis that nearly always reproduces sexually. We show that when N. cinerea females do reproduce asexually, offspring are genetically identical to their mothers. However, asexual reproduction is limited to a nonrandom subset of the genotypes in the population. Only females that have a high level of heterozygosity are capable of parthenogenetic reproduction and there is a strong familial influence on the ability to reproduce parthenogenetically. Although the mechanism by which genetic variation facilitates asexual reproduction is unknown, we suggest that heterosis may facilitate the switch from producing haploid meiotic eggs to diploid, essentially mitotic, eggs.     

Evolutionary implications of developmental instability in parthenogenetic Drosophila mercatorum. II. Comparison of two strains with identical genotypes,but different modes of reproduction

Developmental instability is particularly pronounced in parthenogenetic strains of Drosophila mercatorum. All parthenogenetically produced eggs in a given strain have the same genotype, but even when reared in the same environment, only approximately 5% of the eggs initiating development ever reach adulthood. A sexual analogue of a parthenogenetic strain was created to investigate the basis of this developmental instability. The two strains have identical genotypes (except for the Y chromosome in males of the sexual strain) and differ only in mode of reproduction. The sexual strain had a much lower rate of developmental instability than the parthenogenetic strain, suggesting that the instability is caused by the mode of reproduction per se and is not due to homozygosity, disruption of coadapted gene complexes, or any other feature of the parthenogenetic genome. The increased rate of abortion with parthenogenetic reproduction is caused by a proportional increase in the normal panoply of errors that occur in sexual reproduction but at a much lower rate. Attempts to establish other sexual analogues of laboratory parthenogenetic strains revealed different male sterility factors within several parthenogenetic genomes that could potentially act to prevent hybridization with sexually reproducing ancestors during the incipient stages in the evolution of an entirely parthenogenetic lineage.     

Do ecological niches differ between sexual and asexual lineages of an aphid species?

According to environmental-based theories on the maintenance of sexual reproduction, sexual and asexual populations may coexist if they occupy different ecological niches. The aphid Rhopalosiphum padi offers a good opportunity to test this hypothesis since sexual and asexual lineages show local coexistence during a large part of their respective life-cycles. Because these two reproductive variants are morphologically identical but genetically distinct, we first characterized them using genetic markers in populations of R. padi in areas where sexual and asexual lineages may occur in sympatry. We then inferred the natal host plant of sexual and asexual genotypes by analysing stable isotopic ratios and showed that sexual ones mostly originated from C₃ Poaceae while asexual ones originated from C₃ and C₄ plants, although the majority came from C₄ Poaceae. These findings indicate that ecological niches of sexual and asexual lineages of R. padi differ, offering a plausible explanation for the local coexistence of the two reproductive modes in this species through habitat specialisation.     

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.     

Seasonal variation of genotypes and reproductive plasticity in a facultative clonal freshwater invertebrate animal (Hydra oligactis) living in a temperate lake

Facultative sexual organisms combine sexual and asexual reproduction within a single life cycle, often switching between reproductive modes depending on environmental conditions. These organisms frequently inhabit variable seasonal environments, where favorable periods alternate with unfavorable periods, generating temporally varying selection pressures that strongly influence life history decisions and hence population dynamics. Due to the rapidly accelerating changes in our global environment today, understanding the population dynamics and genetic changes in facultative sexual populations inhabiting seasonal environments is critical to assess and prepare for additional challenges that will affect such ecosystems. In this study, we aimed at obtaining insights into the seasonal population dynamics of the facultative sexual freshwater cnidarian Hydra oligactis through a combination of restriction site‐associated sequencing (RAD‐Seq) genotyping and the collection of phenotypic data on the reproductive strategy of field‐collected hydra strains in a standard laboratory environment. We reliably detected 42 MlGs from the 121 collected hydra strains. Most of MLGs (N = 35, 83.3%) were detected in only one season. Five MLGs (11.9%) were detected in two seasons, one (2.4%) in three seasons and one (2.4%) in all four seasons. We found no significant genetic change during the 2 years in the study population. Clone lines were detected between seasons and even years, suggesting that clonal lineages can persist for a long time in a natural population. We also found that distinct genotypes differ in sexual reproduction frequency, but these differences did not affect whether genotypes reappeared across samplings. Our study provides key insights into the biology of natural hydra populations, while also contributing to understanding the population biology of facultative sexual species inhabiting freshwater ecosystems.     

Could different environmental conditions select for different flight characteristics in sexual and asexual parasitoid Venturia canescens?

In the parasitoid Venturia canescens Gravenhorst (Hymenoptera: Ichneumonidae), asexual and sexual wasps coexist in the field in the Mediterranean basin, but only the asexual strain is present indoors. The sexual strain dominates outdoors despite the demographic costs associated with the production of males and mate location. The present study tests whether females of the sexual and asexual strains of V. canescens differ in flight characteristics in line with the differences of their preferred habitats and enquires whether these differences might contribute to the persistence of sexually reproducing individuals in the vicinity of asexual counterparts. The results show that sexual female wasps are smaller than their asexual counterparts. The size of wasps has a strong influence on flight parameters, with larger animals generally being better fliers. In wasps of approximately the same size, sexual wasps fly faster than their asexual counterparts under experimental laboratory conditions, in terms of both the average speed over the observation period as well as the longest single flight. Sexual wasps also perform fewer flights to cover the same distance. Sexual wasps have higher wing loading than asexual ones of the same size, which could have contributed to the observed differences in speed between individuals of both reproductive modes. There are no significant differences between the two reproductive modes in the parameters related to the distance traversed or the time spent in flight. This study shows clear differences in the flight behaviour of sexual and asexual V. canescens. Together with previous results, this finding suggests differential adaptations to their preferred habitats. These differences might ease the competition between modes of reproduction through niche and habitat differentiation and might help to explain their coexistence on a geographical scale.     

EVOLUTION OF TRADE-OFFS BETWEEN SEXUAL AND ASEXUAL PHASES AND THE ROLE OF REPRODUCTIVE PLASTICITY IN THE GENETIC ARCHITECTURE OF APHID LIFE HISTORIES

Life‐history theory postulates that evolution is constrained by trade‐offs (i.e., negative genetic correlations) among traits that contribute to fitness. However, in organisms with complex life cycles, trade‐offs may drastically differ between phases, putatively leading to different evolutionary trajectories. Here, we tested this possibility by examining changes in life‐history traits in an aphid species that alternates asexual and sexual reproduction in its life cycle. The quantitative genetics of reproductive and dispersal traits was studied in 23 lineages (genotypes) of the bird cherry‐oat aphid Rhopalosiphum padi, during both the sexual and asexual phases, which were induced experimentally under specific environmental conditions. We found large and significant heritabilities (broad‐sense) for all traits and several negative genetic correlations between traits (trade‐offs), which are related to reproduction (i.e., numbers of the various sexual or asexual morphs) or dispersal (i.e., numbers of winged or wingless morphs). These results suggest that R. padi exhibits lineage specialization both in reproductive and dispersal strategies. In addition, we found important differences in the structure of genetic variance–covariance matrices ( G ) between phases. These differences were due to two large, negative genetic correlations detected during the asexual phase only: (1) between fecundity and age at maturity and (2) between the production of wingless and winged parthenogenetic females. We propose that this differential expression in genetic architecture results from a reallocation scheme during the asexual phase, when sexual morphs are not produced. We also found significant G × E interaction and nonsignificant genetic correlations across phases, indicating that genotypes could respond independently to selection in each phase. Our results reveal a rather unique situation in which the same population and even the same genotypes express different genetic (co)variation under different environmental conditions, driven by optimal resource allocation criteria.