The induction of normal and teratoid viviparae by a juvenile hormone and kinoprene in two species of aphids

ABSTRACT. Topical application of a juvenile hormone (JH1) and the JH mimic, kinoprene, to short-day, ovipara-producers of Megoura viciae usually leads to the production of oviparous/viviparous intermediate forms in the progeny sequence, in place of the expected sexual females (oviparae). The ovaries of these abnormal forms may contain embryos rather than the haploid yolky eggs of oviparae; 'mixed' ovaries containing both haploid eggs and embryos are also observed. The intermediates range in form from winged (alate) to wingless (apterous). The fully alate individuals usually contain only parthenogenetic ovaries but differ from the naturally occurring alate viviparae in that they are invariably infertile, have fewer antennal sense organs and often bear pheromone releasing glands on the metathoracic tibiae. The hormonally induced production of normal viviparae is difficult in this species but has been achieved by rearing short-day aphids on kinoprene-treated bean plants.
In Aphis fabae similar oviparous/viviparous teratomorphs have been reported and, in addition, single JH1 treatments were shown to induce normal viviparae at the end of the progeny sequence. Multiple applications, beginning prenatally and continuing through the postnatal development of the gynopara (winged ovipara-producer), showed that the numbers of viviparae born were related to the earliness of the treatment and to the dosage. The results are compared with the effect of a switch in photoperiod and discussed in relation to the endocrine control of aphid polymorphism.     

Reproductive, morphological and behavioural affinities between the alate gynopara and virginopara of the aphid, Aphis fabae

ABSTRACT. 'Normal' alate virginoparae reared under long day conditions (LD 16:8) with postnatal crowding, and 'normal' gynoparae reared in un-crowded, short day conditions (LD 12:12) over two generations were compared in respect of the morph of the progeny, the frequency distribution of secondary rhinaria (placoid sensilla) on the third and fourth antennal segments, and preferred larviposition sites. Although in Aphis fabae the two morphs closely resemble one another morphologically, they differed in each of the above characters. Progeny sequences were analysed after transfer to the opposite photoperiodic regime at various times during postnatal development of the alate mothers. Transfer of presumptive gynoparae from short to long days induced the appearance of virginoparous progeny even when the transfer was made just after the final moult. Transfer of presumptive alate virginoparae from long to short days was effective in inducing oviparous offspring, only if the transfer was made during the first instar; oviparae were always first born. Intermediates between oviparae and viviparae were found at the time when the morph of the progeny changed. Transfer from long to short days also induced gynopara production but there appeared to be an intrinsic mechanism which prevented exclusive gynopara production by alates. When first instar, presumptive gynoparae were transferred to long days, the resulting adults would be described both reproductively and behaviourally as alate virginoparae; the opposite switch, of presumptive alate virginoparae to short days, resulted in adult gynoparae on the same criteria. However, the numbers of secondary rhinaria were influenced more by the prenatal than by the postnatal photoperiodic regime. There was an asymmetry of response in that a switch from short to long days had a greater effect on all three characters monitored than did the opposite switch from long to short days.     

Production of males and gynoparae by apterous viviparae of Myzus persicae continuously exposed to different scotoperiods

At 18–19°C, apterous viviparae of a holocyclic strain of Myzus persicae raised from birth under constant scotoperiods of 9 hr 26 min–15 hr darkness per diem deposited apterous viviparae, alate viviparae, and males, in that sequence. Under the shortest scotoperiod (9 hr 26 min) in which males were recorded, only a few were deposited at the end of reproduction. With increasing duration of the scotoperiods, the aphids switched to the exclusive deposition of males progressively earlier in their reproductive lives. Thus more males and fewer females were produced; however the proportion of wingless females increased. Similar trends were recorded when the number of prenatal exposures to each scotoperiod was increased from 0 to 7.Alatae developed into gynoparae at scotoperiods of 10 hr 29 min or longer, and into virginoparae at 9 hr 40 min or shorter scotoperiods. Gynoparae and alate virginoparae, as well as alates that produced both oviparae and viviparae were found at 10 hr and 10 hr 15 min.When apterous viviparae were transferred to scotoperiods of 10 hr 29 min or 15 hr only when they attained adulthood, they also deposited males but only toward the end of their reproductive lives.     

Effects of some metabolic inhibitors on flowering of Lemna gibba G3, a long-day duckweed

Flowering of Lemna gibba G₃, a long-day duckweed, was inhibitedby adding CuSO₄, AgNO₃, HgCl₂, Na₂WO₄ or iodoacetamide to themedium at the concentrations inducing long-day flowering inLemna paucicostata 6746, a short-day duckweed. This suggeststhat these metabolic inhibitors affected the photoperiodic sensitivityrather than directly affecting flower initiation. Ferricyanidepromoted flowering in both of these short-day and long-day duckweeds. (Received July 7, 1977; )     

Photoperiodic Control of Developmental Diapause in Nymphs of Prostriate Ixodid Ticks (Acari: Ixodidae)

Extrinsic control of developmental diapause in nymphs of prostriate ticks of the subgenus Ixodes sensu stricto (Ixodes ricinus and Ixodes persulcatus from Eurasia and Ixodes scapularis from North America) appears to be based on a complex two-step photoperiodic reaction of a short-day/long-day type. Diapause control in the subgenus Afrixodes (the South African tick Ixodes rubicundus) appears to be based on a simple long-day reaction. The option between non-diapause development and diapausing arrest in engorged nymphs is determined by both pre- and post-feeding photoperiodic regimes. Consequently diapausing arrest in engorged nymphs of Ixodes sensu stricto can be induced either by a short-day (after their engorgement) or by a long-day regime (in unfed nymphs), while active, non-diapause development is possible only when the short-day pre-feeding regime is followed by a long-day post-feeding regime. The photoperiodic response in I. (Afrixodes) rubicundus nymphs seems to be of the long-day type both before and after feeding. Consequently this non-diapause development is enabled by a long-day regime, while diapause is induced by a short-day regime of exposure. Nevertheless, there are some indications that the control of nymphal diapause in the latter species is also of a complex nature. This revised version was published online in July 2006 with corrections to the Cover Date.     

Induction of diapause in the pupa of Phalaenoides glycinae by a hormone from the suboesophageal ganglion

The pupal diapause in Phalaenoides glycinae is facultative, and diapause is induced when larvae are reared in short days at low temperatures. By varying the stimulus and especially by changing larvae from one régime to the opposite during their development it is possible to induce diapause covering a wide and continuous spectrum of intensity. Wounding tends to intensify the diapause if it already exists no matter how weakly, but superficial wounding will not put a strongly non-diapausing individual into diapause. In P. glycinae diapause is caused by a hormone secreted by the suboesophageal ganglion. It is suggested that the intensity of the diapause depends on the concentration of the hormone and the duration of the period that the target (the neurosecretory cells of the brain) remains vulnerable. It is suggested that the suboesophageal ganglion may have the function of secreting a diapause-inducing hormone quite generally in short-day and long-day insects with facultative diapause and in species with obligate diapause as well.     

Male production by apterous viviparae of the aphid Myzus persicae temporarily exposed to different scotoperiods

Male production by apterous viviparae of a holocyclic biotype of the green peach aphid, Myzus persicae, was induced by pre-natal and/or post-natal exposures to a long-night regime of 15 h dark per diem. When the apterae were exposed to three or more long nights immediately after birth and they subsequently developed under a short-night regime of 8 h dark per diem, they produced females (mostly alate viviparae) during the first 8–10 days of reproduction and a high proportion of males thereafter. When the apterae were exposed to two long nights immediately before their birth and to short nights thereafter, they produced relatively few females (mostly alate viviparae), and males were deposited already after 4–6 days of reproduction, i.e. 16–18 days after the first exposure to the long nights. The proportion of males among the progeny of these apterae was highest when the two prenatal exposures comprised scotophases of 11–15 h; under such long-night regimes many aphids switched to producing males exclusively. To achieve this effect, the two long scotophases had to be separated by a photophase of more than 1–2 h. Fewer males were produced and most of the apterae reverted to the production of females (apterous viviparae) when the duration of the two prenatal scotophases was 9 h 45 min-10 h 30 min, or 18 h and longer.One long night of 15–39 h could also induce temporary male production if the aphids were exposed to it late in the 4th larval instar or as teneral adults.     

Parental control of sex ratio in Gammarus duebeni,an organism with environmental sex determination

Parental sex ratio control was investigated in Gammarus duebeni, an amphipod with an environmentally mediated sex determining system. The effect on the F2 generation sex ratio of the photoperiodic conditions experienced by a) the P generation during and after copulation, b) the F1 generation before and after sex determination, and c) the F2 generation themselves during the period of sex determination, was tested. The photoperiodic conditions the F2 generation experienced during the period of sex determination had a significant effect on their sex ratio (more males were produced under long-day than under short-day conditions), but the photoperiodic conditions experienced by the F1 generation males and females or the P generation on the F1 male's side had no effect on the F2 sex ratio. However, the photoperiodic conditions the P generation on the F1 female's side experienced significantly affected the F2 sex ratio. When these animals experienced long-day conditions the F2 generation became female biased and when they experienced short-day conditions, male biased. It is proposed that the mechanism of control operates through the F1 generation mothers whilst in an embryonic stage of development in the P generation mother's brood pouch. The photoperiodically mediated effects of the embryonic F1 generation mother and the F2 generation on sex determination are additive. A mechanism by which both F1 generation maternal and F2 generation sex ratio control could operate in the field is proposed.     

Circadian clock regulates photoperiodic responses governed by distinct output pathways in the bean bug,Riptortus pedestris

Effects of RNA interference (RNAi) targeted against circadian clock genes on two distinct types of photoperiodic responses – ovarian development and lipid accumulation – were investigated in a bean bug Riptortus pedestris, to explore which physiological process in the photoperiodic response involved the circadian clock. Ovarian development and lipid accumulation are known to be regulated by distinct output pathways. Control insects showed clear photoperiodic responses; i.e. induction of ovarian development and suppression of lipid accumulation under long-day conditions, whereas opposite characteristics under short-day conditions. We found that RNAi directed against period, a negative element of the circadian clock, produced a long-day effect for both the ovarian development and lipid accumulation, while RNAi directed against Clock, a positive element of the circadian clock, produced a short-day effect for both, irrespective of photoperiod. These results indicate that the circadian clock comprised of these genes regulates a process governing both distinct photoperiodic responses.     

Sexual forms of the pea aphid, Acyrthosiphon pisum, produced on an artificial diet

In recent years a number of aphid species have been successfully reared on chemically defined diets (Dadd & Mittler, 1966; Auclair, 1965; Dadd & Krieger, 1967; Ehrhardt, 1968). The development of such diets has offered an opportunity to study in detail several aspects of the physiology of these insects. In particular, the composition of the artificial diet has been shown to influence the production of winged forms by Myzus persicae (Sulzer) (Mittler & Dadd, 1966; Dadd, 1968). In all studies thus far, the aphids have been maintained in the parthenogenetic condition in order to accumulate data concerning the growth and fecundity of females of successive generations. However, it was clearly of interest to determine whether sexual forms could be produced by diet-reared aphids. If so, further information regarding the sexual reproduction of these insects would be forthcoming. Attempts to achieve this using local strains of Myzus persicae, Aphis fabae Scopoli and Acyrthosiphon pisum (Harris) were unsuccessful, presumably because these strains were anholocyclie (Kunkel, unpubl.). A clone of a green strain of A. pisum, previously found to be holocyclic (Sutherland, unpubl.), was then obtained from England and was cultured at 20° C in a photoperiodic regime of 16 hr light: 8 hr dark per day on young bean plants (Vicia faba). The artificial diet on which the experimental aphids were maintained was formulated according to Dadd (1967) and enclosed in sachets of stretched parafilm (Dadd, Krieger & Mittler, 1967). The aphids were provided with fresh sachets every 3–4 days. Adult apterous females taken from the plant culture were caged in groups of five, and exposed to a photoperiodic regime of 10 hr light: 14 hr dark per day at 15°. Successive batches of larvae deposited by these aphids were maintained in this environment until they were adult and had produced offspring for several days. These developed into oviparae and males. Compared to the sexual forms produced on host plants, these diet-reared individuals grew relatively poorly and mortality was high. Nevertheless, the surviving oviparae deposited numerous eggs, but these remained pale green whereas viable, fertilized eggs deposited by plant-reared oviparae rapidly become black. In the case of aphids reared on host plants in a short-day environment the possibility exists that the photoperiod may act indirectly via the plants and not directly on the insects themselves — a doubt which has been raised concerning Megoura viciae Buckton (von Dehn, 1967). However, our results with A. pisum reared on artificial diet demonstrate, as Lees did for M. viciae (Lees, 1960, 1967), that it is unnecessary to implicate the host plant in the determination of males and oviparae. This does not, of course, exclude the possibility that photoperiod-induced changes in a host plant may play a role as well. Nor have we ruled out the possibility that dietary composition may influence the aphids directly or their response to other environmental stimuli leading to the production of sexual forms.     

The photoperiodic responses and phenology of an English strain of the pea aphid Acyrthosiphon pisum

Abstract. 1. The response curves for the photoperiodic induction of the sexual forms (oviparae and males) differ significantly in an English clone of the pea aphid Acyrthosiphon pisum Harris. Male production is sharply peaked. The late summer scotophases (dark periods) that initiate male production are 1.0–1.5 h shorter than those that initiate ovipara production; the induction of males, but not oviparae, virtually ceases at scotophases longer than 12 h. This disparity suggests that there are two photoperiodic clocks.
2. All ovipara-producing aphids switch spontaneously to virginopara production part-way through the progeny sequence, irrespective of photoperiod. This may confer the ability to overwinter partheno-genetically under favourable climatic conditions. Since males are always born last in the progeny sequence this possibility would be pre-empted unless the terminal male sequences were suppressed by long winter scotophases.
3. The role of the photoperiodic response in determining the seasonal phenology was tested in the field by exposing a succession of laboratory-reared aphids to natural photoperiods, in late summer and autumn. Adult males and oviparae developed synchronously in early October, the difference in critical scotophase compensating for the late appearance of males in the progeny sequence. A large part of the 'civil twilight' is photoperiodically active.
4. Clones propagated outdoors by isolating aphids in each generation from the terminal sequence of virginoparae did not survive the whole winter of 1985/86. The chances of survival were reduced by severe weather and by the inability of the photoperiodic system to 'turn off' the production of early born oviparae which are, therefore, 'wasted'.     

Embryogenesis and the production of males by apterous viviparae of the green peach aphid Myzus persicae in relation to photoperiod

Apterous viviparae of a holocyclic strain of Myzus persicae were given various numbers of prenatal and postnatal exposures to male-inducing, long-night scotophases (15 hr darkness per diem). The sex of the embryos in various positions within their ovarioles was determined from chromosome preparations and correlated with the sequence with which female and male larvae were deposited. An abnormal follicle was found frequently between the female and male embryos in the ovarioles of aphids raised under long nights.Apterous viviparae exposed to long nights from birth or earlier usually produced several females and then switched over to exclusive male production. The more prenatal exposures to long nights given to the aphids, the fewer females were deposited by them and the earlier they started to produce males. When apterae were continuously exposed to long nights from 2 days or more before their birth, some, and occasionally all, their ovarioles were solely androparous. In general, male-producing apterae deposited considerably fewer larvae (female as well as male) than apterae that produced females exclusively. The 1–2 day pause in larviposition that typically occurs between the deposition of the female and male larvae was attributed to a slower rate of development of the male embryos. The results are discussed in relation to the hormonal changes that may be induced by the photoperiodic treatments.     

Temperature and Photoperiodic Control of Development in the Green Shield Bug Palomena prasina (L.) (Heteroptera,Pentatomidae) in Leningrad Province

Thermal reaction norms for development (the lower temperature threshold, temperature sensitivity, and sum of degree-days) can show phenotypic plasticity in response to a combination of ecological factors. The goal of this study was to evaluate the degree of plasticity of the thermal reaction norms for development under different photoperiodic conditions in the green shield bug Palomena prasina. Experiments were conducted in 2015 and 2016. In 2015, two photoperiodic regimens (12 and 22 h of light per day) and five constant temperatures (20, 22, 24, 26, and 28°C) were used; a lower temperature of 16°C was added in 2016. There were no differences in the egg developmental time between the two photoperiodic conditions and across the two experiments. Under the short-day photoperiodic regimen, nymphal development was faster at all the temperatures and was characterized by greater thermal sensitivity and a higher temperature threshold than under the long-day photoperiod. Besides, the relationship between the developmental rate and temperature deviated from linearity at 26 and 28°C under short-day conditions. The adaptive nature of the observed nymphal response to photoperiodic conditions was confirmed by our phenological observations and an outdoor cage experiment. The adult body mass slightly increased with rising temperature under short-day conditions but did not depend on the temperature under long-day ones. Females were larger than males, and both sexes had a greater body mass under long-day conditions than under short-day ones. In 2015, the eggs for experiments were collected before mid-July, almost a month later than in 2016. Nymphs that hatched from the later eggs (in 2015) had significantly higher relative growth rates than the early-season nymphs (in 2016) at 20, 22, and 24°C under both photoperiods. This discrepancy between years was probably related to the maternal effect, namely, the difference in the female physiological age.

     

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.     

The photoperiodic induction of ovarian diapause in the cabbage whitefly, Aleyrodes proletella (Homoptera: Aleyrodidae)

Female cabbage whitefly, Aleyrodes proletella L., overwinter in ovarian diapause. A scoring system for ovarian development has proved valuable in following the progress of diapause and has revealed a marked difference between the effects of stationary short-day treatment and one involving a transfer from long-day to short-day photoperiods. The former results in a weak inhibition of ovarian development, whilst the latter completely inhibits pre-emergence oögenesis and greatly retards post-emergence development. Therefore, A. proletella may be regarded as a long-day-short-day species. Peak photoperiodic sensitivity is located in the third instar, although some degree of sensitivity is present for most of larval development. The inductive effect of 10 short-day cycles, at the time of peak sensitivity, is not abolished by subsequent long-day treatment.     

Inhibition by kinoprene of photoperiod-induced male production by apterous and alate viviparae of the aphid Myzus persicae

Photoperiod-induced male production by apterous and alate viviparae of the green peach aphid. Myzus persicae, was reduced or prevented by treating the aphids with the JH analog kinoprene (Zoecon's insect growth regulator ZR 777). Concomitant with this reduction in the number of males was an increase in the production of females. This was most clearly demonstrated for apterous viviparae that had been raised from birth under weak long-night regimes of 10–10.5 hr dark day, and exposed to 0.1% kinoprene-treated radish seedlings for 2–3 days on reaching the fourth larval instar or adulthood.Male production by alate viviparae, whose apterous mothers were born and raised for 5 days under a long-night regime of 15 hr dark day and then maintained under a short-night regime of 8 hr dark day, was completely inhibited by exposing them to kinoprene-treated plants for 2–3 days when they had reached the fourth instar.It is concluded that the kinoprene treatment affects sex chromosome replication in the oögonia of an aphid so that these germ cells develop parthenogenetically into females (2n = 12 with two X chromosomes) rather than males (2n = 11 with one X chromosome). This may result either from a direct action of absorbed kinoprene on the oögonia or from an indirect action whereby the kinoprene stimulates the insect's hormonal system to produce a hormone that stimulates development of the oögonia into females.     

THE INDUCTION OF FLOWERING IN NICOTIANA. II. PHOTOPERIODIC ALTERATION OF THE CHLOROGENIC ACID CONCENTRATION

Chlorogenic acid and its 2 isomers, believed to be the 4– and 5–0-caffeoylquinic acids, have been extracted from leaves of photoperiodic species of Nicotiana, separated by column chromatography (gradient elution) and measured quantitatively during the course of photoperiodic induction. In both N. tabacum cultivar ‘Maryland Mammoth’ (a short-day plant) and N. sylveslris (a long-day plant), the change of the meristem from the vegetative to the flowering shape is preceded by a rise in the chlorogenic acid content of the leaves. During the differentiation of the flower primordia in the shoot apex, there is a drop in the concentration of the chlorogenic acid in the leaves, which is especially marked in the short-day species. The levels of the 2 isomers decrease also at that time. There is no change in the ratios of the 3 caffeoylquinic acids during photoperiodic induction. In both the long- and the short-day species, the 3-isomer (chlorogenic acid) is present at the highest concentration. In the short-day species, there is more of the 4-isomer than of the 5-isomer, whereas in the long-day species, the level of the 5-isomer equals or surpasses that of the 4–0-caffeoylquinic acid.     

Short-day experience is not a prerequisite for the termination of photorefractoriness in the reproductive cycle of baya weaver,Ploceus philippinus

In most photoperiodic avian forms (irrespective of temperate or tropical distribution) including the baya weaver,Ploceus philippinus, seasonal reproduction comes to an end due to the development of a photoperiodically controlled photorefractory phase when birds cease to respond to the stimulatory effect of long days. In the present paper photoperiodic control of the termination of photorefractory phase has been examined by studying the effect of short-day exposure lasting 4–6 months on long-day response of birds. Results indicate that unlike in other photoperiodic birds short-day exposure of winter is not a prerequisite for the termination of photorefractory phase in the reproductive cycle of baya weaver. Artificial long days on the other hand hasten the termination of this phase. Refractory phase in baya weaver, therefore, unlike that in temperate forms, is a temporary state resulting most likely from a sequel of physiological events triggered by long days of spring/summer which temporarily mask the photostimulatory response. Spontaneous termination of photorefractoriness in birds of tropical habitats may have a selective value imparting to the reproductive cycle the necessary elasticity for adaptation to diverse ecological conditions.     

CAM induction by photoperiodism in green callus cultures from a CAM plant

Abstract Green calli obtained from leaves of the CAM-inducible plant Kalanchoe blossfeldiana cv. Montezuma were grown either under long-day or short-day regimes in the Phytotron of Gif-sur-Yvette. Callus cells were found to be CAM inducible by the short-day treatment, according to levels and diurnal oscillations of malate pools and phosphor-enolpyruvate (PEP) carboxylase (EC.4.1.1.31) capacity. De novo synthesis of PEP carboxylase was shown to occur under the short-day regime. In spite of continuous net CO² output, CAM-like patterns of CO₂ exchange by calli were obtained under the short-day treatment. After 2 months under both photoperiodic conditions, spontaneous organogenesis in callus tissues gave rise to numerous shootlets which were determined as photoperiod dependent for CAM; the same was so for plants originating from these shootlets.