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.     

Evidence that mass trapping suppresses pink bollworm populations in cotton fields

Both thelytokous and arrhenotokous Trichogramma minutum were collected from eggs of the spruce budmoth, Zeiraphera canadensis in New Brunswick, Canada and their phenotypic traits compared for use in biological control. The lower threshold temperature for development of thelytokous and arrhenotokous parasitoids was 9.7 and 10.1 °C, respectively; the former required significantly higher degree-days for development from egg to adult (–x±SE=165.1±5.8 °D) than the latter (128.1±4.9 °D). Thelytokous and arrhenotokous parasitoids had similar forewing length (0.49±0.01 vs. 0.49±0.01 mm) and adult lifespan (13.3±0.7 vs. 14.0±1.1 days), but significantly different fecundity and sex ratios. Thelytokous females produced fewer offspring (89.5±6.6 vs. 173.9±6.4) and fewer female progeny (77.2±5.4 vs. 109.8±3.3) despite an overall higher proportion of females (91.6±1.1% vs. 65.4±2.8%) than their arrhenotokous counterparts. Ovarian dissections showed that the number of eggs increased with parasitoid age in arrhenotokous parasitoids but remained steady in thelytokous parasitoids. The variation in ovarian development of the two forms was the major factor contributing to the differences in fecundity. Thelytokous parasitoids were more host-specific than arrhenotokous ones; when offered eight host species, the former rejected three whereas the latter rejected only one. Thelytokous parasitoids survived better than arrhenotokous ones when stored from 30 to 150 days at 4 °C. Thelytokous females were slower at initiating flight after emergence than arrhenotokous females but maintained flight activity longer (6 h). These results indicate that thelytokous T. minutum are different from their arrhenotokous counterparts physiologically, biologically and ecologically and that they may play different roles in the field. The potential for using thelytokous parasitoids in biological control programs is discussed.     

Selection in the absence of males does not affect male-female conflict in the parasitoid wasp Leptopilina clavipes (Hymenoptera: Figitidae)

Divergent reproductive interests of males and females can lead to sexually antagonistic coevolution (SAC). In the absence of males, adaptations evolved under SAC are released from selection and expected to deteriorate. In this study, we investigated this prediction using two populations of the parasitoid wasp Leptopilina clavipes, one arrhenotokous and one thelytokous. Thelytokous females were induced to produce sons by curing them of their Wolbachia-infection. We examined whether thelytokous males were less able to inhibit female remating than arrhenotokous males and whether thelytokous females were more susceptible to male-induced longevity reduction than arrhenotokous females. The results showed that females were monandrous, regardless of whether mated with an arrhenotokous or thelytokous male. While ongoing courtship of males reduced female life span, there was no longevity cost of mating for either arrhenotokous or thelytokous females. Our results therefore do not support the idea that adaptations evolved under SAC deteriorate under prolonged female-only selection.     

Development of a multiplex method to discriminate between Neochrysocharis formosa (Hymenoptera: Eulophidae) reproductive modes

A multiplex polymerase chain reaction (PCR) method was applied to differentiate thelytokous and arrhenotokous strains of Neochrysocharis formosa (Westwood). Alignment of strain first internal transcribed spacer regions revealed high nucleotide variability and the strain-specific primer sequence used. Strains were easily differentiated after gel electrophoresis of multiplex PCR products because arrhenotokous specimens produced a 500-bp fragment as well as the 800-bp fragment common to both strains. This method successfully distinguished N. formosa strains regardless of collection site across Japan; thus, it is probably suitable for similar applications in Turkey, Italy, and elsewhere.     

The biosystematic relations between a thelytokous and an arrhenotokous form ofAphytis mytilaspidis (Le Baron) [Hymenoptera: Aphelinidae]

Biological and morphological characters of the thelytokous and arrhenotokous forms ofA. mytilaspidis and their hybrids were investigated. Some biological differences between the thelytokous and arrhenotokous forms were found. The former is adapted to warmer condition and will parasitizeHemiberlesia lataniae as well asDiaspis echinocacti, while the latter will not parasitizeH. lataniae. The overall fecundity of the thelytokous form is lower than that of the arrhenotokous form, whereas the “effective fecundity”, female progeny per female parent, is higher in the thelytokous form. Apart from the no. of setae in the wings delta, there are no distinguishing morphological characters between the arrhenotokous and thelytokous forms.     

Biological Control Potential of Wolbachia -infected Versus Uninfected Wasps: Laboratory and Greenhouse Evaluation of Trichogramma cordubensis and T. deion Strains

The effects of thelytoky-inducing Wolbachia ( &#102 -proteobacteria) on Trichogramma cordubensis and T. deion (Hymenoptera, Trichogrammatidae) were studied in laboratory and greenhouse conditions. One infected (thelytokous, all female) line of each wasp species was compared with its conspecific uninfected (arrhenotokous, sexual) counterpart for several fecundity and dispersal traits. Arrhenotokous lines had a higher fecundity than their thelytokous counterparts, which suggests that Wolbachia negatively affect the fecundity of Trichogramma females. The arrhenotokous females dispersed more in the laboratory than their thelytokous counterparts. In the greenhouse, the opposite effect or no difference between lines was found, indicating that the laboratory set-up used to measure dispersal is not useful to predict relative dispersal of the females in the greenhouse. Calculations show that by releasing 100 adult wasps of both lines, thus including arrhenotokous males in the sexual line, more eggs are parasitized by the thelytokous wasps. Therefore, in spite of their lower individual female fecundity, thelytokous lines have a better potential for biological control than their arrhenotokous counterparts.     

The biosystematic relations between a thelytokous and an arrhenotokous form ofAphytis mytilaspidis (Le Baron) [Hymenoptera: aphelinidae] I. The Reproductive relations

The reproductive relations and the probability of hybridization between an arrhenotokous and a thelytokous form ofA. mytilaspidis were investigated so as to determine the significance of thelytoky in biosystematic studies and its value as a taxonomic character. Gene markers were utilized to detect and follow the various phases of the introgressive process between the arrhenotokous and thelytokous forms. The two forms show only a partiel sexual isolation, the major barrier is prezygotic, arrhenotokous males are much less efficient in recognizing the thelytokous female and copulating with them. A thelytokous female, once inseminated, will utilize the sperm as efficiently as the arrhenotokous female. Viable and fertile hybrids are produced and when conditions are favorable and a suitable host is present the introgressive process will result in a hybrid swarm. The hybrids acquire traits carried by both ancestral stocks.     

Negative evidence of parthenogenesis induction by Wolbachia in a gallwasp species, Dryocosmus kuriphilus

The alpha‐proteobacteria of the genus Wolbachia is a widespread group of maternally inherited endosymbionts of arthropod and nematode hosts. Wolbachia infection induces a range of host phenotypes, including cytoplasmic incompatibility, male killing, feminization, and induction of thelytokous parthenogenesis. Heterogony (cyclical parthenogenesis) is a remarkable characteristic of oak gallwasps, Cynipini, the largest tribe of the Cynipidae. A few species of Cynipini are exceptional in that they are univoltine and exhibit thelytokous parthenogenesis, probably because they lost the arrhenotokous generation of their heterogonic ancestor species due to Wolbachia infection. In this study, the presence of Wolbachia was detected using polymerase chain reaction primers for the wsp genes in a thelytokous parthenogenetic species [Dryocosmus kuriphilus (Yasumatsu)] (Hymenoptera: Cynipidae: Cynipini). Approximately 29.8 and 87.1% of adults of the Zhuzhou and Fuzhou strains, respectively, were infected with Wolbachia while all females of the remaining four strains collected from other localities in China were Wolbachia free. The length of the wsp fragment of Zhuzhou and Fuzhou strains was found to be 573 and 561 bp, respectively. The nucleotide sequence of the bacterial wsp fragment indicated that the endosymbiotic bacteria of the Zhuzhou and Fuzhou strains are members of supergroup A, but belong to different clades; they probably originated from two independent infection events. In conclusion, thelytokous parthenogenesis of D. kuriphilus is not caused by Wolbachia infection and the deletion of the arrhenotokous generation is thus not associated with such an infection.     

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.     

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.     

Reduced sexual functionality of PI‐Wolbachia‐infected females of Tetrastichus coeruleus

Wolbachia are endosymbiotic bacteria known to manipulate the reproduction of their hosts by, for example, inducing parthenogenesis. In most cases of Wolbachia‐induced parthenogenesis, the infection is fixed and the entire host population consists of females. In the absence of males and sexual reproduction, genes involved in sexual reproduction are not actively maintained by selection. Accumulation of neutral mutations or selection against maintenance of sexual traits may lead to their loss or deterioration. In addition, females may lose the ability to reproduce sexually due to ‘functional virginity mutations’ that may spread concomitantly with the Wolbachia infection through a population. The parasitoid wasp Tetrastichus coeruleus (Nees) (Hymenoptera: Eulophidae) forms an ideal model to study the decay of sexual functionality, because it has both Wolbachia‐infected, parthenogenetic populations and uninfected, sexual populations. We compared several components of sexual functionality of arrhenotokous (sexual) and thelytokous (parthenogenetic) T. coeruleus females. First, we tested whether arrhenotokous and thelytokous females were equally attractive and receptive to males. Second, we examined whether mating is costly to females by measuring the life span of mated and virgin females. Last, we studied the morphology of the spermathecae of arrhenotokous and thelytokous females. Mated females had shorter life spans than virgin females, showing that mating carried a fitness cost. Two sexual traits of thelytokous females have degraded compared to arrhenotokous females. Arrhenotokous and thelytokous females were equally attractive to males, but thelytokous females were unreceptive to males. Furthermore, there was a clear difference in spermathecal morphology between arrhenotokous and thelytokous females. Our data do not allow distinction between the various potential causes of such degradation. Although the longevity cost of mating may indicate selection against the maintenance of costly sexual traits, accumulation of neutral mutations, functional virginity mutations, manipulation by Wolbachia, and/or the genetic distance between the two populations may all have contributed to the decay of sexual traits in thelytokous females.     

Are individuals from thelytokous and arrhenotokous populations equally adept as biocontrol agents? Orientation and host searching behavior of a fruit fly parasitoid

Hymenopteran parasitoids generally reproduce by arrhenotoky, in which males develop from unfertilized eggs and females from fertilized eggs. A minority reproduce by thelytoky, in which all-female broods are derived from unfertilized eggs. Thelytokous populations are potentially of interest for augmentative biological control programs since the exclusive production of females could significantly lower the costs of mass rearing. Behavioral traits are a major component of parasitoid efficacy. Here, we examined orientation and host searching behavior in thelytokous and arrhenotokous populations of the fruit fly parasitoid Odontosema anastrephae Borgmeier (Hymenoptera: Figitidae). Orientation behavior to various odorant sources was studied in a two-choice olfactometer. No major differences were found between thelytokous and arrhenotokous wasps for this behavior. However, when host-searching behaviors were analyzed, some differences were found. Thelytokous females arrived sooner, foraged longer, and remained longer on non-infested guavas than arrhenotokous females. Individuals of both forms exhibited similar stereotyped behavioral sequences vis-à-vis guava treatments, with only slight deviations detected. Our results suggest that individuals from selected thelytokous and arrhenotokous O. anastrephae populations have similar abilities to search for tephritid larvae, supporting the use of thelytokous strains for augmentative releases.     

Biotic performances of thelytokous and arrhenotokous strains of <Emphasis Type="Italic">Thrips tabaci</Emphasis> (Thysanoptera: Thripidae) showing resistance to cypermethrin

Two distinct reproductive types of Thrips tabaci Lindeman, one thelytokous and one arrhenotokous, have been shown to develop target-insensitive cypermethrin resistance conferred by sodium channel mutation (T929I). In this study, we examined the relation between cypermethrin resistance and biotic performances of these reproductive types. Among the T. tabaci strains examined, resistant arrhenotokous strains became adults more quickly after hatching than resistant thelytokous strains. Female adults of resistant thelytokous strains exhibited shorter longevity and oviposited fewer eggs than those of susceptible strains of the same reproductive type. Resistant arrhenotokous strains exhibited similar longevity and fecundity to susceptible thelytokous strains. We further examined the relation between reproductive types and T929I using a total of 85 strains. All 53 arrhenotokous strains encoding T929I were judged to be cypermethrin resistant. Among 32 thelytokous strains with T929I, only four were regarded as cypermethrin resistant. Based on the results, we discuss possible mechanisms accounting for the recent prominence of arrhenotoky T. tabaci in Japan.     

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.     

不同温度下松毛虫赤眼蜂孤雌产雌品系和两性生殖品系对米蛾卵的寄生功能反应

赤眼蜂部分蜂种或品系受Wolbachia侵染营孤雌产雌生殖。 通过室内试验分析了在4个恒温（20, 25, 30和35℃）下松毛虫赤眼蜂Trichogramma dendrolimi两性生殖品系和孤雌产雌品系对米蛾Corcyra cephalonica卵的寄生功能反应, 旨在比较不同温度两品系的寄生功能反应差异, 评价孤雌产雌品系在生物防治中的应用潜力。 结果表明： 松毛虫赤眼蜂两个品系对米蛾卵寄生作用均随寄主密度的增加而增大;随温度的升高松毛虫赤眼蜂两品系的功能反应类型由Ⅲ型改变为Ⅱ型。孤雌产雌品系以30℃的处置时间最短(0.0207 d), 最大日寄生量为48.31粒卵, 其次是25℃, 35℃最小;两性生殖品系以25℃的处置时间最短(0.0188 d), 最大日寄生量为53.08粒卵, 其次是30℃, 20℃最小; 松毛虫赤眼蜂两品系的寄生功能反应存在显著差异, 30℃下孤雌产雌品系为Ⅱ型功能反应而两性生殖品系为Ⅲ型。 从处置时间来看, 20℃时两品系无显著性差异(P≥0.05), 在25℃和35℃孤雌产雌品系寄生米蛾卵时花费的时间显著长于两性生殖品系(P<0.05), 而30℃却相反。 可见, 寄主密度、 温度和Wolbachia影响松毛虫赤眼蜂功能反应。     

The cytological basis for reproductive variability in the Anoetidae (Sarcoptiformes: Acari)

Meiosis is described in a thelytokous strain of the anoetid mite Histiostoma feroniarum (Dufour) and in both sexes of the arrhenotokous strain of this species. Oogenesis in the thelytokous strain is accomplished by ameiotic mitosis with only one pseudo-maturation division. During this division one or more chromosomes may move to the poles precociously and while in this position can be mistaken for centrioles. Fourteen chromosomes are found at metaphase of the pseudo-maturation division and in cleaving eggs of this strain. In the arrhenotokous strain, male meiosis consists of a single mitotic division. Oogenesis is regular and 7 bivalents are observed at the first maturation division. Metaphases of the first cleavage division in fertilized eggs show 14 chromosomes and 7 chromosomes in unfertilized eggs.It is postulated that the thelytokous strain has arisen from the arrhenotokous strain. This assumption is in agreement with that suggested for several insect species previously reported. The evolution in the Acari and the variability in the modes of reproduction in this suborder are discussed in light of the findings in this paper on the Anoetidae.     

The influence of temperature and host availability on the host exploitation strategies of sexual and asexual parasitic wasps of the same species

In the hymenopteran parasitoid Venturia canescens, asexual (obligate thelytoky not induced by Wolbachia bacteria) and sexual (arrhenotokous) wasps coexist in field conditions despite the demographic cost incurred due to the production of males by sexual females. Arrhenotoky predominates in field conditions, whereas populations in indoor conditions (mills, granaries) are exclusively thelytokous. These differences in the relative abundance of the two modes of reproduction between environments suggest that the individuals of each reproductive mode may have developed strategies adapted to the conditions prevailing in each kind of habitat. The two environments contrast in temperature variability and in the spatial heterogeneity of host availability. In this study, we considered the combined effect of temperature and host availability on host patch exploitation by thelytokous and arrhenotokous V. canescens. As expected, arrhenotokous females were more sensitive to temperature changes. If the temperature decreased before foraging, they remained longer and exploited patches more thoroughly. This is consistent with the expected behaviour of parasitoids in response to signs of unfavourable conditions that entail increasing risk of time limitation or a reduced probability of attaining further patches. Both arrhenotokous and thelytokous females increased patch exploitation with host availability. However, unexpectedly, we found no difference in the way the two types of wasp responded to differences in host availability. Differences in the strategies adopted under different environmental conditions may indicate divergence of niche-specific life history traits between the two modes of reproduction. Niche displacement may partly account for the coexistence of these two modes of reproduction at a geographical scale.     

Biological comparisons between arrhenotokous and thelytokous biotypes ofMesochorus nigripes [Hym.: Ichneumonidae]

The host preferences and sex ratios ofMesochorus biotypes from Sweden and Colorado (U.S.A.) were studied in the field and laboratory. TheseMesochorus are secondary parasites ofBathyplectes spp., parasites ofHypera postica (Gyllenhal). The Colorado biotype is 100% thelytokous, and clearly prefersBathyplectes stenostigma (Thomson) as a host. Only an arrhenotokous biotype was positively detected in Sweden, and it appeared to preferB. curculionis (Thomson). However, some of the data suggest that the thelytokous biotype was probably also present in Sweden, at least inB. stenostigma. The behavioral differences and reproductive isolation of the thelytokous and arrhenotokous biotypes indicate that they are separate sibling species, even though they cannot yet be separated morphologically, and isozyme analyses were inconclusive (possibly due to a mixture of biotypes in Sweden).      

The dynamics of energy allocation in adult arrhenotokous and thelytokous Venturia canescens

The ability to adjust resource allocation to the quality of the environment has broad implications for animal reproductive success. Organisms with complex life cycles that may experience various selection pressures during their lifetime are expected to evolve mechanisms to modulate the resource allocation strategies adopted during ontogeny to the conditions encountered by the adult. In the parasitoid Venturia canescens Gravenhorst (Hymenoptera: Ichneumonidae), thelytoky appears to have been selected for in anthropogenic habitats, where hosts are relatively numerous and food is absent, and arrhenotoky in natural habitats where hosts are more scarce and food is present. A previous study postulated that during their juvenile stage, females of both reproductive modes adopt strategies of energy allocation in accordance with these conditions, possibly providing a direct short‐term advantage to arrhenotokous forms, which partially co‐occur with thelytokous forms under natural conditions. To test this assumption, we provided daily adult thelytokous and arrhenotokous females with a small number of hosts together with food. To compare their lifetime resource allocation strategies, we recorded wasp longevities, egg loads, and carbohydrate reserves in wasps of different ages. Our analysis indicates that thelytokous females are able, to a certain extent, to cope with these conditions, because they reached the same longevity as arrhenotokous females. Nevertheless, thelytokous females suffered from a higher degree of time limitation compared with arrhenotokous ones, and arrhenotokous wasps appeared to maintain their energetic advantage over the adult stage. These results provide new insights, and point to the consideration of other activities, such as flight performance and/or ability to reach food and hosts, in the understanding of the role of resource allocation strategies in the maintenance of sex in this species.