Multiple Wolbachia determinants control the evolution of cytoplasmic incompatibilities in Culex pipiens mosquito populations

Wolbachia are maternally inherited endosymbionts that can invade arthropod populations through manipulation of their reproduction. In mosquitoes, Wolbachia induce embryonic death, known as cytoplasmic incompatibility (CI), whenever infected males mate with females either uninfected or infected with an incompatible strain. Although genetic determinants of CI are unknown, a functional model involving the so-called mod and resc factors has been proposed. Natural populations of Culex pipiens mosquito display a complex CI relationship pattern associated with the highest Wolbachia (wPip) genetic polymorphism reported so far. We show here that C. pipiens populations from La Réunion, a geographically isolated island in the southwest of the Indian Ocean, are infected with genetically closely related wPip strains. Crossing experiments reveal that these Wolbachia are all mutually compatible. However, crosses with genetically more distant wPip strains indicate that Wolbachia strains from La Réunion belong to at least five distinct incompatibility groups (or crossing types). These incompatibility properties which are strictly independent from the nuclear background, formally establish that in C. pipiens, CI is controlled by several Wolbachia mod/resc factors.     

Wolbachia affects oviposition and mating behaviour of its spider mite host

Wolbachia bacteria are transmitted from mother to offspring via the cytoplasm of the egg. When mated to males infected with Wolbachia bacteria, uninfected females produce unviable offspring, a phenomenon called cytoplasmic incompatibility (CI). Current theory predicts that ‘sterilization’ of uninfected females by infected males confers a fitness advantage to Wolbachia in infected females. When the infection is above a threshold frequency in a panmictic population, CI reduces the fitness of uninfected females below that of infected females and, consequently, the proportion of infected hosts increases. CI is a mechanism that benefits the bacteria but, apparently, not the host. The host could benefit from avoiding incompatible mates. Parasite load and disease resistance are known to be involved in mate choice. Can Wolbachia also be implicated in reproductive behaviour? We used the two‐spotted spider mite – Wolbachia symbiosis to address this question. Our results suggest that uninfected females preferably mate to uninfected males while infected females aggregate their offspring, thereby promoting sib mating. Our data agrees with other results that hosts of Wolbachia do not necessarily behave as innocent bystanders – host mechanisms that avoid CI can evolve.     

Contrasting effects of Wolbachia on cytoplasmic incompatibility and fecundity in the haplodiploid mite Tetranychus urticae

Recent studies on Wolbachia‐induced incompatibility in haplodiploid insects and mites have revealed a diversity of cytoplasmic incompatibility (CI) patterns among host species. Here, we report intraspecific diversity in CI expression among four strains of the arrhenotokous mite Tetranychus urticae and in T. turkestani. Variability of CI expression within T. urticae ranged from no CI to complete CI, and included either female embryonic mortality or male conversion types of CI. A fecundity cost attributed to the infection with the high‐CI Wolbachia strain was the highest ever recorded for Wolbachia (?80 to ?100% decrease). Sequence polymorphism at a 550‐bp‐portion of Wolbachia wsp gene revealed two clusters distant by 21%, one of which included three Wolbachia strains infecting mite populations sampled from the same host‐plant species, but showing distinct CI patterns. These data are discussed in the light of theoretical predictions on the evolutionary pathways followed in this symbiotic interaction.     

Environmental effects on cytoplasmic incompatibility and bacterial load in Wolbachia-infected Drosophila simulans

The effects of high temperatures, antibiotics, nutrition and larval density on cytoplasmic incompatibility caused by a Wolbachia infection were investigated in Drosophila simulans. Exposure of larvae from an infected stock to moderate doses of tetracycline led to complete incompatibility when treated females were crossed to infected males; the same doses only caused a partial restoration of compatibility when treated males were crossed to uninfected females. In crosses with treated females, there was a strong correlation between dose effects on hatch rates and infection levels in embryos produced by these females. Ageing and rearing males at a high temperature led to increased compatibility. However, exposing infected females to a high temperature did not influence their compatibility with infected males. Male temperature effects depended on conditions experienced at the larval stage but not the pupal stage. Exposure to 25 °C reduced the density of Wolbachia in embryos compared with a 19 °C treatment. Low levels of nutrition led to increased compatibility, but no effect of larval crowding was detected. These findings show the ways environmental factors can influence the expression of cytoplasmic incompatibility and suggest that environmental effects may be mediated by bacterial density.     

Geographic variations and combining abilities in the two-spotted spider mite, Tetranychus urticae

Geographic variations and combining abilities of three fitness traits: the mean number of offspring, and the mean number and proportion of female offspring, in the two-spotted spider mite were investigated using four widely separated strains of Tetranychus urticae Koch. Analyses of data obtained from a complete set of diallel crosses, involving the four strains, revealed large and highly significant specific combining abilities and reciprocal effects in all the fitness characteristics examined. It was concluded that the whole chain of reproductive events, from egg production of parental females to the fertility of hybrid daughters could be severely affected by incompatibility between parental populations.

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Résumé L'étude a porté sur les différences géographiques et les combinaisons de trois caractères adaptatifs—nombre moyen de descendants, nombre moyen et proportion de femelles dans la descendance—sur quatre souches différentes de Tetranychus urticae. L'analyse des données obtenues à partir d'un lot complet de croisements dialléliques, sur les quatre souches, révèle pour tous les caractères adaptatifs examinés une forte aptitude à l'association et aux effets réciproques. On peut en conclure que la chaîne totale des événements intervenant dans la reproduction—de la production d'oeufs par les mères jusqu'à la fécondité des filles hybrides—pourrait être fortement modifiée par l'incompatibilité entre populations parentales.

     

短时高温暴露对Q型烟粉虱存活和生殖适应性的影响

在室内将Q型烟粉虱Bemisia tabaci Q-biotype成虫在44℃下暴露1 h后观察成虫的存活率、产卵量、雌雄寿命和后代存活能力,以研究短时高温暴露对Q型烟粉虱生物学特性的影响。结果表明,Q型烟粉虱成虫在44℃下暴露1 h后的存活率为43.5%,暴露热激后的单头雌虫的产卵量为77.2粒,低于常温下(26℃)的产卵量(100.1粒);短时高温可显著缩短Q型烟粉虱成虫的寿命,在44℃下暴露1 h后Q型烟粉虱雌雄虫寿命分别为14.5 d和10.2 d,显著低于常温下(26℃)雌虫20.4 d和雄虫18.2 d;短时高温对Q型烟粉虱后代存活率和雌雄性比无显著影响,但其产卵高峰期延迟,产卵持续期缩短。以上结果表明,短时高温热激可影响Q型烟粉虱的生殖情况,造成Q型烟粉虱产卵量降低和寿命缩短,Q型烟粉虱雌虫耐热性强于雄虫。     

No variation for Wolbachia-induced hybrid breakdown in two populations of a spider mite

Wolbachia are cytoplasmically transmitted bacteria that infect several species of mites. In the two-spotted spider mite Tetranychus urticae Koch this symbiont can induce reproductive incompatibility. Wolbachia-induced reproductive incompatibility is observed in crosses between Wolbachia-infected (W) males and uninfected (U) females. This incompatibility is expressed in F1 broods as male-biased sex ratios, an effect called cytoplasmic incompatibility (CI). However, in the two-spotted spider mite, Wolbachia-induced reproductive incompatibility may extend to the F2: broods of virgin F1 females from U×W crosses sometimes suffer increased mortality rates. This F2 effect is called hybrid breakdown (HB). Several isofemale lines derived from mites collected from rose and cucumber plants had been previously tested for CI. Here we report on the results obtained for HB.     

DNA sequences and cross-breeding experiments in the hawthorn spider mite Amphitetranychus viennensis reveal high genetic differentiation between Japanese and French populations

Sequence variation of the complete second internal transcribed spacer (ITS2, 445 bp) of nuclear ribosomal DNA and part of the mitochondrial cytochrome oxidase I gene (COI, 350 bp) was examined in Amphitetranychus viennensis (Zacher) mites (Acari:Tetranychidae) from four French and four Japanese locations. Sequence analysis consistently revealed the separation of the samples in two major groups: French mites differed from Japanese by 3.8–4.1% of the nucleotide divergence in COI sequences. These two groups also displayed distinct ITS2 consensus sequences (2.1% nucleotide divergence). A few variations, not affecting the diagnostic sites around the consensus sequence, were revealed among cloned copies of the same individual. Reciprocal crosses and backcrosses between one French and two Japanese populations disclosed strong reproductive incompatibility. However, fertile hybrid females were obtained, indicating the conspecificity of the tested mites. Despite the presence of Wolbachia in the French strain, but not in the Japanese ones, our crosses did not display the unidirectional incompatibility typically produced by this microorganism, but rather a bidirectional – although asymmetrical – incompatibility pattern. The post-zygotic incompatibilities in A. viennensis cannot be explained by the presence of Wolbachia but to some extent by mite genome divergence resulting from limited gene exchange between allopatric populations. Experiments of Wolbachia elimination by antibiotic treatment and subsequent crosses with cured strains are still needed to fully understand the reproductive incompatibility patterns in this mite species.     

The paternal sex ratio chromosome induces chromosome loss independently of Wolbachia in the wasp Nasonia vitripennis

 The paternal sex ratio chromosome (PSR) is a paternally-inherited supernumerary chromosome found in some males of Nasonia vitripennis. PSR induces the loss of N. vitripennis’s paternal autosomes in early fertilized embryos. Previous examinations have not directly addressed the complication of PSR’s co-occurrence with Wolbachia. Wolbachia is the name assigned to a group of cytoplasmic bacteria which induce numerous reproductive alterations in their hosts. In Nasonia, Wolbachia cause cytoplasmic incompatibility (CI) which also results in paternal chromosome loss. Here we address the question of whether PSR’s function (i.e. PSR’s transmission and/or ability to induce chromosome loss) depends upon or interacts with Wolbachia. A strain of PSR males is artificially cleared of Wolbachia. Test crosses and cytological observations of this strain demonstrate that PSR’s transmission and ability to induce chromosome loss is not dependent upon Wolbachia. Comparisons suggest an absence of interactions between PSR and Wolbachia when they co-occur. Fluorescent and confocal microscopy are used to examine and compare early embryos. Observations demonstrate that microtubule interactions with chromatin do not appear to cause the initial loss of the paternal chromosomes. Cytological observations presented here also differ from previous reports of PSR- and Wolbachia-induced chromosome loss. Received: 3 May 1996 / Accepted: 24 June 1996     

Environmental condition related reproductive strategies and sex ratio in hydras

Kaliszewicz, A. and Lipińska, A. 2011. Environmental condition related reproductive strategies and sex ratio in hydras. —Acta Zoologica (Stockholm) 00 :1–7. Temperature and food supply appeared to affect sex ratio, sex composition and percentage of sexual individuals in three Hydra species: Hydra vulgaris, Hydra circumcincta and Hydra viridissima. We found three sexes present: females, males and hermaphrodites depending on environmental conditions. Hydra vulgaris appeared to be a species with a temperature‐dependent sex determination (TSD). The males and hermaphrodites were present only under rising temperatures, whereas females were observed exclusively at lowering temperatures. Hydras reproduced asexually at constant room temperature. Unlimited food affected sex ratios and induced the presence of males in H. circumcincta at lowering temperatures. Thus, H. circumcincta may be recognised as another Hydra species in which sex is determined by environmental factors (ESD). Under rising temperatures, the number of hermaphroditic individuals was higher when food supply was unlimited in all three species, indicating that hermaphrodites may need more energy to produce both male and female gonads. Both temperature changes and food supply positively affected asexual reproductive strategies in hydras, especially budding rates. Hydra circumcincta appeared to be less agile than other hydras and able to self‐fertilise. It is likely that self‐fertilisation is an adaptation to the low probability of meeting a mate belonging to the other clone.     

Diapause induction and termination in the predatory mite Euseius finlandicus in peach orchards in northern Greece

The course of diapause induction as well as of diapause termination infemales of the predatory mite Euseius (Amblyseius)finlandicus Oudemans (Acari: Phytoseiidae) in Northern Greece wasdetermined by transferring females during winter and early spring from peachtrees to a short day (LD 8:16) or a long day (LD 16:8) photoperiod both at 20°C. The first diapause females were found in mid September andby the first week of October all the females were in diapause. The mean numberof days required for diapause termination under the short day photoperiod LD8:16 was gradually reduced from 93.7 days in the beginning of October to lessthan 20 days in mid February and early March. Under the long day photoperiod ofLD 16:8 diapause was terminated in less than 20 days irrespective of the dateof collection. These results indicate that by mid February photoperiodicsensitivity of females was lost and diapause was terminated. However, femaleswere found in their overwintering sites until the second half of March,probablybecause of the prevailing relatively low temperatures and lack of adequatefood.     

Sorting out the effects of Wolbachia, genotype and inbreeding on life-history traits of a spider mite

Wolbachia bacteria manipulate host reproduction by inducing cytoplasmic incompatibility (CI) and sex ratio distortion. Wolbachia are transmitted from mother to offspring through the cytoplasm of the egg. Therefore, reproduction of Wolbachia is tightly coupled to reproduction of its host. Mathematical analysis predicts that in the course of evolution, traits that reduce the physiological costs of the infection will be selectively favored. For a Wolbachia-host system to evolve, traits under selection must have some genetic component and variation must be present in the population. We have previously established that highly inbred isofemale lines of the two-spotted spider mite Tetranychus urticae may differ regarding the effects of infection by Wolbachia, and that at least some of the traits affected had a genetic component. However, the effects measured could have been affected by the fact that the lines were severely inbred prior to the experiments. In this paper we attempt to distinguish between the effects of Wolbachia, isofemale line, and inbreeding. We show that Wolbachia did not affect longevity but infected females produced smaller clutch sizes, more daughter-biased sex ratios and had decreased F1 mortality; between-line variation was found for clutch size, F1 mortality and sex ratio; finally, inbreeding resulted in an overall reduction of clutch sizes, and a change in survival curves and mean longevity. This revised version was published online in July 2006 with corrections to the Cover Date.     

Culled males,infant mortality and reproductive success in a pre-industrial Finnish population

Theoretical and empirical literature asserts that the sex ratio (i.e. M/F) at birth gauges the strength of selection in utero and cohort quality of males that survive to birth. We report the first individual-level test in humans, using detailed life-history data, of the ‘culled cohort’ hypothesis that males born to low annual sex ratio cohorts show lower than expected infant mortality and greater than expected lifetime reproductive success. We applied time-series and structural equation methods to a unique multigenerational dataset of a natural fertility population in nineteenth century Finland. We find that, consistent with culled cohorts, a 1 s.d. decline in the annual cohort sex ratio precedes an 8% decrease in the risk of male infant mortality. Males born to lower cohort sex ratios also successfully raised 4% more offspring to reproductive age than did males born to higher cohort sex ratios. The offspring result, however, falls just outside conventional levels of statistical significance. In historical Finland, the cohort sex ratio gauges selection against males in utero and predicts male infant mortality. The reproductive success findings, however, provide weak support for an evolutionarily adaptive explanation of male culling in utero.     

Variable host quality, life-history invariants, and the reproductive strategy of a parasitoid wasp that produces single sex clutches

The parasitic wasp Achrysocharoides zwoelferi (Hymenoptera, Eulophidae) produces clutches consisting of only one sex. Moreover,male clutch size is invariably one while female clutches arein the range one to four. We designed field experiments todetermine the effect of host quality on clutch composition.We found that solitary male and solitary female clutches werereared from the same size mines, and that larger mines tendedto produce gregarious female clutches. A higher proportionof male clutches were placed in older hosts, despite theirlarge size. Variation in body size, both between and withinclutches, was measured in order to test the predictions of models that take into account the constraint that clutch size is aninteger trait, something of potential importance when absoluteclutch size is low. Our data supported several predictionsof these models, including the trade-off-invariant rule foroptimal offspring size developed by Charnov and Downhower.However, while most invertebrate clutch size models assume equal resource share among members of the same clutch, we found anincrease in inequality in larger clutches.     

Expression of cytoplasmic incompatibility in Drosophila simulans and its impact on infection frequencies and distribution of Wolbachia pipientis

The aim of this study is to examine the expression of cytoplasmic incompatibility and investigate the distribution and population frequencies of Wolbachia pipientis strains in Drosophila simulans. Nucleotide sequence data from 16S rDNA and a Wolbachia surface protein coding sequence and cytoplasmic incompatibility assays identify four distinct Wolbachia strains: wHa, wRi, wMa, and wAu. The levels of cytoplasmic incompatibility between six lines carrying these strains of bacteria and three control lines without bacteria are characterized. Flies infected with wHa and wRi are bidirectionally incompatible, and males that carry either strain can only successfully produce normal numbers of offspring with females carrying the same bacterial strain. Males infected with wAu do not express incompatibility. Males infected with the wMa strain express intermediate incompatibility when mated to females with no bacteria and no incompatibility with females with any other Wolbachia strain. We conduct polymerase chain reaction/restriction fragment length polymorphism assays to distinguish the strain of Wolbachia and the mitochondrial haplotype to survey populations for each type and associations between them. Drosophila simulans is known to have three major mitochondrial haplotypes (siI, sill, and siIII) and two subtypes (siIIA and siIIB). All infected lines of the sil haplotype carry wHa, wNo, or both; wMa and wNo are closely related and it is not clear whether they are distinct strains or variants of the same strain. Infected lines with the silIA haplotype harbor wRi and the siIIB haplotype carries wAu. The wMa infection is found in siIII haplotype lines. The phenotypic expression of cytoplasmic incompatibility and its relation to between-population differences in frequencies of Wolbachia infection are discussed.     

Effect of temperature on the reproductive biology of Peristenus spretus (Hymenoptera: Braconidae), a biological control agent of the plant bug Apolygus lucorum (Hemiptera: Miridae)

Peristenus spretus Chen et van Achterberg (Hymenoptera: Braconidae), a parasitoid of the plant bug Apolygus lucorum (Hemiptera: Miridae), has been studied for use in augmentative biological control in China. Under laboratory conditions, we explored the development, survival, age-specific and potential lifetime fecundity, oviposition period and progeny sex ratio of P. spretus reared at six constant temperatures (15°C, 19°C, 23°C, 27°C, 31°C, 35°C) on the second instar nymphs of A. lucorum. At 15°C, male and female P. spretus took 48.7 ± 0.3 and 52.5 ± 0.3 days to complete their immature development, while developmental time was reduced by more than half at 23°C and 27°C. The parasitoid can only develop to the larval stage at 31°C and neither larva nor pupa survived at 35°C. The estimated lower developmental threshold of the immature stage was 7.3°C. When parasitoid adults were exposed at 15°C, females laid 90% of their eggs at first 19 days of oviposition and had an extended reproductive life. In contrast, females held at 27°C laid most of their eggs (90%) in their first of 10 days of oviposition and had shorter longevity. The highest potential lifetime fecundity of P. spretus was 671.2 ± 34.7 SE eggs produced over 23.4 ± 1.4 SE days at 23°C. At 15°C, 19°C and 23°C, sex ratios of reared parasitoids were male-biased, but at 27°C there was no male bias.     

Photoperiodic control of adult diapause in the predacious mite, Amblyseius potentillae: repeated diapause induction and termination

ABSTRACT. Photoperiodic control of facultative reproductive diapause was examined in females of the phytoseiid mite, Amblyseius potentillae (Garman). Full diapause was induced by rearing the mites from egg to adult under short-day photoperiods. Egg-laying females, however, which had experienced a long-day photoperiodic regime during pre-imaginal development, could still be induced to enter diapause when they were transferred to a short-day regime. Diapause development proceeded slowly under a short-day photoperiod, but was accelerated under long days. During diapause development under short days the photoperiodic sensitivity of the females diminished gradually and ultimately disappeared completely. However, after completion of diapause, sensitivity to photo-period reappeared. A second diapause could be induced in post-diapause females under short-day photoperiods and completed again under long-day photoperiods. These results show that A. potentillae remains sensitive to diapause-inducing and diapause-averting daylengths during the adult stage and that a second diapause may be induced after completion of the first one.