Sexual Morph Production Research Articles

Identification of Aphis coronillae (Hemiptera: Aphididae) clones with anholocyclic life cycle

AbstractThis study examined the life history traits of Aphis coronillae Ferrari (Hemiptera: Aphididae) clones collected in Utsunomiya City, Tochigi Prefecture, eastern Japan. Results showed that the collected clones are classifiable into two life cycle forms: holocyclic and anholocyclic. No significant difference in nymphal development, fecundity, or adult longevity was observed between holocyclic and anholocyclic clones. Results also indicated that photoperiod and temperature affect sexual morph production in holocyclic clones.

Transcriptomic changes in the pea aphid, Acyrthosiphon pisum: Effects of the seasonal timer and photoperiod

Many insect species use photoperiod as a cue for induction of seasonal responses, including seasonal polyphenism. Although most aphid species viviparously produce parthenogenetic and sexual morphs under long and short days, respectively, a seasonal timer suppresses the sexual morph production over several successive generations during a few months following hatching of a sexually produced diapause egg. To reveal the relative influences of photoperiod and the seasonal timer on the reproductive polyphenism at the gene expression level, we performed RNA sequencing-based transcriptome analyses in the pea aphid, Acyrthosiphon pisum (Hemiptera: Aphididae). Under short days, aphids with an expired seasonal timer showed a higher expression level in hundreds of genes than those with an operative seasonal timer. In contrast, aphids with an operative seasonal timer did not show upregulation in most of these genes. Functional annotations based on gene ontology showed that histone modifications and small non-coding RNA pathways were enriched in aphids with an expired seasonal timer under short-day conditions, suggesting that these epigenetic regulations on gene expression might be involved in a mechanism of maternal switching from the parthenogenetic to sexual morph production.

Suppression of autumnal sexual morph production in spring by a seasonal timer in an aphid

AbstractPhotoperiod is the major seasonal cue for phenotypic plasticity in the regulation of development and reproduction. Aphids have a peculiar mechanism in which sensitivity to the photoperiod is lost for a few months through successive generations after hatching from diapause eggs, and therefore, the mechanism responsible for the photorefractory period is termed “a seasonal timer”. However, whether the seasonal timer has adaptive significance has never been investigated. Here, we show that the photorefractory generation avoids an unseasonal sexual morph production under short days in spring in the pea aphid, Acyrthosiphon pisum (Harris). When the seasonal timer operated, the overwintered generation, stem mothers, produced only parthenogenetic progenies under natural photoperiods and temperatures in both warm and cold springs. After repeated parthenogenesis following diapause, however, aphids with an expired seasonal timer produced sexual females and males typical of autumn under natural photoperiods and temperatures in a warm spring. These sexual morphs are thought to have a reproductive disadvantage compared to parthenogenetic morphs in the following summer. We thus conclude that the seasonal timer is adaptive for avoiding sexual morph production in spring. The present study shows, for the first time, that a photorefractory period lasting over generations is a trait of ecological importance.

Clonal variation of sexual morph production in response to temperature and photoperiod in soybean aphid, Aphis glycines (Hemiptera: Aphididae)

The life cycle of Aphis glycines Matsumura (Hemiptera: Aphididae) has been recognized as holocyclic. This study examined photoperiod and temperature effects on fecundity and sexual morph production using six A. glycines clones collected in northern, eastern, western, and southern Japan. Results showed that the six clones included anholocyclic and intermediate ones. Low temperature and short photoperiod negatively affected fecundity, except for one clone with anholocyclic life cycle. Possible mechanisms for the year-round parthenogenetic production of the anholocyclic clone are discussed.

Effects of temperature and photoperiod on the production of sexual morphs of Aphis gossypii (Hemiptera: Aphididae) in Jeju, Korea

This study was conducted to quantify the effects of photoperiod and temperature on the production of sexual morph of A. gossypii. Photoperiod and temperature unequivocally affected the production of sexual morphs of A. gossypii. The transition rate of A. gossypii to sexual morphs was increased with decreasing day lengths. No gynoparae or males were induced in 13hday length at temperatures between 15 and 24°C. No sexual morphs were observed at temperature above 21°C regardless of the day length. We have provided a predicted percentile curves of sexual morph occurrence in relation to photoperiod and temperature. Using this model, critical day lengths at 50% production rate of sexual morphs were calculated to be 12.34, 12.32 and 12.11h at 14, 16 and 18°C, respectively. The model output predicted well the first male occurrence in the field. Also, this density curve should be useful to understand population dynamics of holocyclic life cycle of A. gossypii in a changing environment.

Delayed setting of the photoperiodic response in recombinant clones of the aphid species Sitobion avenae

1. To explore the possible causes of apparent changes in reproductive mode from obligate to cyclical parthenogenesis over time in recombinant clones of the aphid Sitobion avenae Fabricius, all F1 progenies from various crosses were tested for several consecutive years for sexual morph production, after several weeks' exposure to a short photoperiod.2. Variable proportions of the F1 progenies from selfing and outcrossing holocyclic clones did not produce mating females when induction was attempted in the year of hatching, but only after further induction, the following year or after. This ‘delayed setting of the photoperiodic response’ (DSPR) was much stronger in recombinants from crosses involving only clones from oceanic regions than in those involving one clone from a region with a continental climate.3. F1 progenies resulting from crosses between one holocyclic and one intermediate clone did not show DSPR. It appeared again in the F2.4. DSPR preferentially affected the latest hatched clones in a given progeny.5. This phenomenon is neither an experimental artefact nor as a result of clone contamination. It appears to be because of a genetically controlled quantitative trait affecting the length of the ‘interval timer’, and may represent an adaptation of holocyclic aphid clones from oceanic regions to unpredictable winter climates.

Juvenile hormone titre and related gene expression during the change of reproductive modes in the pea aphid

Most aphids show reproductive polyphenism, i.e. they alternate their reproductive modes from parthenogenesis to sexual reproduction in response to short photoperiods. Although juvenile hormone (JH) has been considered a likely candidate for regulating the transition from asexual to sexual reproduction after photoperiod sensing, there are few studies investigating the direct relationship between JH titres and the reproductive-mode change. In addition, the sequencing of the pea aphid genome has allowed identification of the genes involved in the JH pathway, which in turn allows us to examine their expression levels in relation to the reproductive-mode change. Using liquid chromatography-mass spectrometry in the pea aphid, JHIII titre was shown to be lower in aphids producing sexual morphs under short-day conditions than in aphids producing parthenogenetic morphs under long-day conditions. The expression levels of genes upstream and downstream of JH action were quantified by real-time quantitative reverse-transcription-PCR across the reproductive-mode change. The expression level of JH esterase, which is responsible for JH degradation, was significantly higher in aphids reared under short-day conditions. This suggests that the upregulation of the JH degradation pathway may be responsible for the lower JHIII titre in aphids exposed to short-days, leading to the production of sexual morphs.

Elimination of a specialised facultative symbiont does not affect the reproductive mode of its aphid host

Abstract 1. Microorganisms that manipulate the reproduction of their hosts through diverse mechanisms including the induction of parthenogenesis are widespread among arthropods.2. The pea aphid, Acyrthosiphon pisum, shows a variation in its reproductive mode, with lineages reproducing by cyclical parthenogenesis (obligate alternation of parthenogenetic and sexual generations each year) and others by obligate parthenogenesis (continuous asexual reproduction all year round). In addition, the pea aphid harbours, along with Buchnera the primary aphid endosymbiont, several facultative symbionts whose prevalence differs among host populations.3. The possible influence of a Rickettsia facultative symbiont on the reproductive mode of its host was tested on two pea aphid clones by comparing the response of infected and uninfected individuals with the same genetic background to conditions that typically induce the production of sexual morphs.4. No significant effect of the Rickettsia infection was found on the type of reproductive morphs produced (sexual vs. asexual) or on their quantities for the two clones.5. However, the Rickettsia had a detrimental effect on the fitness of its aphid host, in apparent contradiction to the high prevalence of this symbiont in some host populations. It is suggested that this negative impact may disappear under specific environmental conditions, transforming a parasitic association into a mutualistic one.

Detection and characterization of new genotypes of Myzus antirrhinii (Hemiptera: Aphididae) in Japan, with evidence for their production of sexual morphs

Two forms of Myzus persicae (Sulzer), F-15 and R306N′, resembling M. antirrhinii (Macchiati) in esterase profile have been found in Japan. To determine the genetic relationship of F-15 and R306N′ with M. antirrhinii, clonal lineages of F-15, R306N′ and those of 14 other forms of M. persicae collected in Japan were analysed for 17 polymorphic microsatellite DNA loci. Two microsatellite multi-locus (MS) genotypes of M. persicae and two MS genotypes, Ma3 and Ma4, of M. antirrhinii from Australia were used as references. The 16 Japanese forms were represented by different MS genotypes. F-15 and R306N′ had, respectively, 44.1% and 35.3% of their alleles at the 17 loci in common with Ma3 and Ma4, and some of the common alleles were peculiar in size. F-15 and R306N′ shared 22.6% and 29.6%, respectively, of their alleles with the other 16 MS genotypes of M. persicae. The corresponding values for Ma3 and Ma4 were both 27.4%. F-15 and R306N′ were grouped reliably with the two Australian MS genotypes of M. antirrhinii both by neighbour-joining method based on shared allele distance and by a Bayesian method with Markov Chain Monte Carlo algorithm. These results suggest that F-15 and R306N′ are genetically closely related to M. antirrhinii and isolated from the gene pool of M. persicae despite their ability to produce sexual morphs. It is therefore proposed that F-15 and R306N′ should be classified as M. antirrhinii.

Detection and characterization of new genotypes of <I>Myzus antirrhinii</I> (Hemiptera: Aphididae) in Japan, with evidence for their production of sexual morphs

Two forms of Myzus persicae (Sulzer), F-15 and R306N', resembling M. antirrhinii (Macchiati) in esterase profile have been found in Japan. To determine the genetic relationship of F-15 and R306N' with M. antirrhinii, clonal lineages of F-15, R306N' and those of 14 other forms of M. persicae collected in Japan were analysed for 17 polymorphic microsatellite DNA loci. Two microsatellite multi-locus (MS) genotypes of M. persicae and two MS genotypes, Ma3 and Ma4, of M. antirrhinii from Australia were used as references. The 16 Japanese forms were represented by different MS genotypes. F-15 and R306N' had, respectively, 44.1% and 35.3% of their alleles at the 17 loci in common with Ma3 and Ma4, and some of the common alleles were peculiar in size. F-15 and R306N' shared 22.6% and 29.6%, respectively, of their alleles with the other 16 MS genotypes of M. persicae. The corresponding values for Ma3 and Ma4 were both 27.4%. F-15 and R306N' were grouped reliably with the two Australian MS genotypes of M. antirrhinii both by neighbour-joining method based on shared allele distance and by a Bayesian method with Markov Chain Monte Carlo algorithm. These results suggest that F-15 and R306N' are genetically closely related to M. antirrhinii and isolated from the gene pool of M. persicae despite their ability to produce sexual morphs. It is therefore proposed that F-15 and R306N' should be classified as M. antirrhinii.

Temporal habitat variability and the maintenance of sex in host populations of the pea aphid

The evolutionary maintenance of sex, despite competition from asexual reproduction, has long intrigued the evolutionary biologists owing to its numerous apparent short-term costs. In aphids, winter climate is expected to determine the maintenance of sexual lineages in the high latitude zones owing to their exclusive ability to produce frost-resistant eggs. However, diverse reproductive modes may coexist at a local scale where climatic influence is counteracted by microgeographical factors. In this study, we tested the influence of local habitat characteristics on regional coexistence of reproductive modes in the pea aphid, Acyrthosiphon pisum. In the laboratory, the induction of sexual morph production of many pea aphid genotypes from the local fields of annual (pea and faba bean) and perennial (alfalfa and red clover) crops in Western France indicated that A. pisum lineages from annual crops had a significantly higher investment in sexual reproduction than A. pisum lineages from the perennial hosts. We propose that temporal habitat variability exerts a selective pressure to maintain the sexual reproduction in A. pisum. The ecological and evolutionary consequences of the association between the mode of reproduction and the host population on gene flow restriction and on ecological specialization are discussed.

Photoperiodic determination of gynoparae and males of damson‐hop aphid Phorodon humuli

Abstract. Sexual morph production in Phorodon humuli is controlled by daylength. Wingless aphids reared from birth in short‐day conditions (LD 12 : 12 h) and transferred when adult to long‐day conditions (LD 18 : 6 h) produce only gynoparae and males until death some 7 weeks later, whereas those reared in long days and transferred to short days produce 20% wingless parthenogenetic females, 50% gynoparae and 30% of males in an overlapping sequence. No winged morph capable of re‐infesting hop is produced. Less mature embryos are more sensitive to short days than older embryos because 100% of the former became gynoparae after 4 days of exposure of their mothers, and 59% when their mothers were exposed for the 4 days immediately preceding the birth of their offspring. Two days of exposure to short days switches 94% of young embryos from wingless to gynopara production when mature. The response to short days is irreversible. Wingless aphids reared from birth to adult in short days produce 30% fewer offspring than those reared to the same stage in long days and are male‐biased, with 76–78% of their offspring being male.

Life‐cycle variation in the aphid Sitobion avenae: costs and benefits of male production

Abstract 1. Patterns of male production and life‐cycle variation were investigated in the aphid Sitobion avenae. Seventy‐seven field‐collected clones were subjected to a 14 °C short day‐length regime to assess their reproductive modes, and three clones were used to study life‐cycle inheritance. A further analysis assessed the cost of male production.2. In comparison with those from East Anglia, there were more holocyclic and intermediate clones found in Scottish populations, and they produced significantly more mating females. In total, 44% of clones were androcyclic.3. The inheritance of life cycle showed a greater level of complexity than could be achieved by previously suggested monohybrid inheritance mechanisms.4. Holocyclic and intermediate clones produced a higher proportion of males than did androcyclic clones. Inter‐clonal differences were reflected in the pattern of male production in the reproductive sequence.5. A significant cost was associated with male production in terms of a reduction in both fecundity and total offspring biomass.6. Winged females rarely gave birth to males but the pattern of mating female production differed between holocyclic and intermediate clones.7. Patterns of male and mating female production by the different types of clone may be related to different advantages and disadvantages of dispersal and inbreeding.8. Recent models of aphid overwintering could be enhanced by consideration of issues raised in this study, such as the cost of male production, the inheritance of life cycle, and the patterns of sexual morph production.

An interval timer controls the production of sexual morphs in Myzus persicae (Homoptera: Aphididae)

Abstract The interval timer mechanism was examined in two clones of Myzus persicae (Sulzer) originating from peach in Naousa, North Greece. Overwintering eggs were collected in April 1997 and after egg hatch the morphs of progeny were recorded at LD 10 : 14 h and 17 °C until the appearance of sexuals. In one clone, observations were continued until the 21st generation after egg hatch. In addition, the production of sexual morphs was examined in two other clones originating from Lehonia, Central Greece, when apterae (wingless females) were transferred from long to short days and 17 °C in the second and eighth generation of parthenogenetic rearing after their collection from peach trees. In clones from Naousa, the first gynoparae appear and comprise 10% of alate (winged) females in the second half of the third generation after egg hatch. The percentage of gynoparae increased in each consecutive generation, reaching 100% in fifth and seventh generations in clones Nb and Na, respectively. First males appeared later than gynoparae, in fifth and sixth generation in clones Nb and Na, respectively. In clone Nb, the number of males, after their appearance in fifth generation, was relatively constant from the sixth to the ninth generation (10.8–12.3). Then a significant increase was observed in the 10th generation, thereafter remaining relatively constant until the 21st generation (18.1–19.8). A similar trend in the number of males produced was observed in clones deriving from Lehonia.

Production of sexual morphs by apterous virginoparae of Myzus persicae (Hemiptera: Aphididae) in relation to pre- and postnatal exposure to short day conditions.

The production of males and females by apterae of a holocyclic clone of Myzus persicae (Sulzer) was studied in the laboratory by transferring apterous virginoparae from long day to short day conditions at different stages of their pre- and post-natal development. Prenatal exposure was also examined in nine additional clones coming from different regions of Greece. By increasing the number of short day cycles at 17 degrees C, the aphids switched to male production earlier and produced more males. The highest mean number of male progeny was observed in apterae that were transferred to short day conditions 13-14 days prenatally. Apterae that were transferred to short day conditions after the fourth nymphal instar produced only females. Apterous virginoparae were produced by aphids that were transferred to short day conditions 0-1 days prenatally or postnatally. Aphids, given short days prenatally or in the first instar, produced alate female progeny that were all gynoparae. The later the instar aphids were transferred to short day conditions the fewer the gynoparae produced among their female progeny. A reduction in the total number of progeny and embryos per ovariole was observed as aphids were transferred to short day conditions in earlier stages of their development. The increase in male production, which follows the increase in the duration of long night exposure, was also observed in the additional eight out of nine examined clones.

Variation Between Clones of Schizaphis graminum (Homoptera: Aphididae) in the Photoperiodic Induction of Sexual Morphs

The production of sexual morphs by the greenbug, Schizaphis graminum (Rondani), in response to long scotophases was studied using eight clones of the aphid from one locality in California, one clone from Nebraska (biotype E), and one from Oklahoma (biotype C). The temporal and quantitative differences found in the polymorphism of these clones confirmed that considerable variability in biological traits exists between aphids from local as well as regional populations. The groupings to which the clones could be assigned on the basis of their photoperiodic responses differed from previous groupings based on performance of the clones on different varieties of sorghum.

Sexual Morph Production by Two Regional Biotypes of Myzus persicae (Homoptera: Aphididae) in Relation to Photoperiod

A biotype of the green peach aphid. Myzus persicae (Sulzer), from Yakima, Wash. (46°34'N) produced gynoparae and males in response to daily scotophases that were 1.0–1.5 h shorter than those needed to induce the production of these morphs by a biotype of M. persicae derived from a more southern latitude (40°N) in Spain. Predictions regarding the production of these morphs under fall conditions in their regions of origin are consistent with field observations in these regions.

Interclonal variation in the photoperiodic response for sexual morph production of Japanese Aphis gossypii Glover (Hom., Aphididae)1

AbstractA total of 58 clones of Aphis gossypii, collected from 21 species within 14 families of plants at 13 localities in Japan, were examined to assess interclonal variation in the sexual morph‐producing ability. From the response to short photoperiod (10L: 14D, 18 °C) the clones examined were classified into 4 life‐cycle forms: holocyclic (24 clones), intermediate (4), androcyclic (9) and anholocyclic (21). Holocyclic clones were terminated within a few generations after transfer to the short‐day condition by producing oviparae and males exclusively, whereas clones of the other 3 forms continued parthenogenetic reproduction, but intermediate and androcyclic clones produced not only viviparous females but also respectively oviparae and males, and males. Some differences were found in the life‐cycle form composition even in small samples from different host plants.ZusammenfassungÜber interklonale Unterschiede bei Aphis gossypii Glover (Hom., Aphididae) binsichtlich der Bedeutung der Phutoperiode für das Hervorbringen von GeschlechtstierenDie interklonale Variation in bezug auf die Erzeugung von Geschlechtstieren wurde anhand von 58 Aphis gossypii‐Klonen untersucht. Die Läuse stammten von 21 verschicdenen Pflanzenarten aus 14 Familien und wurden in 13 verschicdenen Gebieten Japans gesammelt. Autgrund ihrer Reaktion auf Kurztagbedingungen (10L:14D; 18°C) wurden die Klone in 4 Lebenszyklus‐Formen unterteilt: holozyklisch waren 24, intermediär 4, androzyklisch 9 und anholozyklisch 21 Klone. Die holozyklischen Klone brachten wenige Generationen nach Beginn der Kurztagbedingungen ausschließlich Oviparae und Männchen hervor. Dagegen blieb bei den anderen 3 Formen die parthenogenetische Fortpflanzung erhalten, aber die intermediären und androzyklischen Klone brachten nicht nur vivipare Weibchen hervor, sondern zusätzlich auch Oviparae und Männchen bzw. nur Männchen. Sogar bei kleinen Stichproben konnten bei den verschiedenen Wirtspflanzen einige Unterschiede in der Zusammensetzung verschiedener Lebenszyklus‐Formen festgestellt werden.

Polymorphism of Biotypes E and C of the Aphid Schizaphis graminum (Homoptera: Aphididae) in Response to Different Scotophases

A comparison was made of the production of sexual morphs by biotypes C and E of the greenbug, Schizaphis graminum (Rondani), when the aphids were raised under different photoperiodic regimes or exposed to long scotophases at different stages in their development. For male production, biotype C required fewer postnatal long-night exposures than biotype E. The threshold (minimal) scotophase for the induction of males in biotype C was 11 h, whereas biotype E required a night length between 11 h 14 min and 11 h 32 min. Ovipara production by both biotypes required a scotophase ≤ 11 h 32 min. The possible ecological significance of the results is discussed.

The winter development, reproduction and lifespan of viviparae of Sitobion avenae (F.) (Hemiptera: Aphididae) on wheat in England

AbstractViviparae of Sitobion avenae (F.) in clip-cages on winter wheat in field plots in southern England were monitored throughout the 1980–81 winter to determine characteristics of development, reproduction and lifespan under winter conditions. Rate-temperature relationships for development and reproduction were well described by straight lines when temperatures were measured above 3°C. A simple thermal-time scale could therefore be used for both processes. The parental morph and the time of year modified thermal-time requirements for the production of an adult's first 20 nymphs but did not affect those for development. For both alatae and apterae, nymph production per day-degree was greater than at higher temperatures and the relationship between reproductive rate and age was different. The minimum temperature experienced by the aphids was −7°C; survival was good, with little low temperature mortality. Total fecundity of apterae was usually greater than at higher temperatures, though some apterae and alatae that were deposited in October had low fecundity, possibly because they were insufficiently acclimatized at the onset of cold winter weather. Overwintering alatae had lower development rates, reproductive rates and total fecundity than apterae and did not survive as long, but were restless as young adults and appeared ready to migrate. Oviparae were produced from late September to mid-October but not after this, suggesting that the clone used could ‘switch off’ sexual morph production in winter.