A review of maternal and embryonic control of phase-dependent progeny characteristics in the desert locust

Hatchlings of the desert locust, Schistocerca gregaria, display phase polyphenism in body coloration and size. This phenomenon has been found to be maternally controlled and two different mechanisms have been proposed to explain the underlying process. One mechanism claims that a water-soluble pheromonal factor secreted by gregarious female adults into the foam plugs of egg pods induces darkening in their progeny. The other mechanism states that hatchling body coloration is pre-determined in the ovaries and that no foam factor is involved in this phenomenon. This mechanism was supported by the observation that hatchling melanization was not prevented by the early washing or separation of eggs, which should have removed the pheromonal factor from the eggs and produced green hatchlings according to the other mechanism. This paper reviews the latest findings related to this phenomenon with special reference to reproductive cycles and genetic differences. The close relationships between egg size and the degree of melanization in hatchlings may provide strong evidence against the possible involvement of the pheromonal factor, because egg size is determined in the ovarioles. Furthermore, the absence of “solitarizing” effects of early washing and separation on hatchling melanization was also confirmed in different genetic strains. A hypothesis proposed by others that such effects occur only in eggs from the first reproductive cycle was tested and rejected. Based on these and other results, a model to explain the mechanisms underlying the maternal control of progeny characteristics and embryonic control of melanization in the hatchling was proposed.     

Phase-related body-color polyphenism in hatchlings of the desert locust, Schistocerca gregaria: re-examination of the maternal and crowding effects

The mechanism controlling the body color of hatchlings was studied for the desert locust, Schistocerca gregaria. A pheromonal factor secreted by gregarious female adults into the foam plugs of egg pods has been suggested to cause darkening in their progeny. We re-examined the role of this maternal factor by washing or separating eggs at deposition. Eggs produced by crowd-reared female adults were washed with saline or separated individually without being washed immediately after deposition and the body color of the hatchlings from them was compared with that from the eggs unwashed and kept in the egg pod until hatching. Most hatchlings were dark and no significant difference was found in the proportions of dark- and light-colored hatchlings between the treatments and controls. Likewise, eggs separated before the foam plug deposition produced dark-colored hatchlings as in the un-separated controls. These results demonstrated that neither washing nor separation of eggs at deposition affected the hatchling body coloration. The variation in hatchling body color was correlated closely to the body weight at hatching, indicating that hatchling body color had been determined maternally. Green hatchlings reared under crowded conditions remained green until the second stadium at which black patterns were induced. It was concluded that body color at hatching has been determined maternally and crowding during the first nymphal stadium influences nymphal body color but its effect is not manifested until the second stadium. The present study casts doubts on the presence of a recently suggested pheromonal factor on the color of the hatchlings.     

Tactile stimuli perceived by the antennae cause the isolated females to produce gregarious offspring in the desert locust, Schistocerca gregaria

Maternal determination of progeny body size and coloration in the desert locust, Schistocerca gregaria, depends on the crowding conditions experienced during the short sensitive period that occurs two to six days before the deposition of the egg pod. Solitarious (isolated-reared) females produce relatively small eggs that yield solitarious green hatchlings but, females that are exposed to crowded conditions during the sensitive period, produce larger eggs that yield the dark-colored hatchlings characteristic of gregarious forms. The present study aimed to determine the stimuli influencing the maternal determination of progeny characteristics as well as the site at which such stimuli are perceived. By exposing isolated female adults to various combinations of visual, olfactory and tactile stimuli from a crowd of other adults, we found that no crowding effects could be elicited without tactile stimulation. Coating of various body surfaces with nail polish followed by exposure to crowding stimulation suggested that female adults perceive crowding stimuli with their antennae. This finding was supported by another experiment in which the antennae were either removed or covered with wax before the isolated females were exposed to crowded conditions. Neither serotonin nor an antagonist of its receptor affected the density-dependent maternal determination of progeny characteristics when injected into isolated or crowded female adults.     

Maternal effects on progeny body size and color in the desert locust, Schistocerca gregaria: examination of a current view

Hatchling body color and size of the desert locust, Schistocerca gregaria, are determined by the population density of the mothers during their reproductive period. Smaller green hatchlings are produced by adults at low population density (solitarious conditions) and larger dark hatchlings at high population density (gregarious conditions). One claim states that a pheromonal factor secreted by gregarious mothers into foam plugs of egg pods induces darkening in hatchlings. Previous research suggests that the foam factor can be removed by separating eggs individually within 1h of deposition, causing presumptive gregarious eggs to hatch without darkening. The present study re-examined this claim and possible factors that have been proposed which could account for the difference between our results and those reported earlier. Early separation was performed on eggs with a low mortality rate. The results showed that the egg separation did not increase the incidence of green hatchlings. Once chorionated in the ovary, eggs remained unchanged in size until the second day after oviposition in either isolated or crowded locusts. This and other results suggest that the phase-dependent differences in body size and color of hatchlings are established in the ovary and that modifications by the accessory gland factor either in the oviduct or after deposition are unlikely.     

Maternal effects on progeny size, number and body color in the desert locust, Schistocerca gregaria: Density- and reproductive cycle-dependent variation

The effects of rearing density and maternal age on the progeny size, number and coloration of the desert locust, Schistocerca gregaria, were investigated. Isolated-reared females deposited smaller, but more eggs than crowd-reared females. The former produced smaller and more eggs with age, whereas the latter showed a tendency to produce larger and fewer eggs over time. A similar tendency was also observed with virgin females, indicating that mating or the presence of males was not important. The first egg pod produced by each mated crowd-reared female contained significantly smaller and more eggs than did the subsequent egg pods. The former often produced many green hatchlings (0-100%) characteristic of solitarious forms, whereas the egg pods deposited after the first pod produced predominantly black hatchlings typical of gregarious forms. Adults were highly sensitive to a shift in rearing density and quickly modified the quality and quantity of their progeny depending on the density encountered. The number of eggs per pod was influenced not only by the mother's rearing density but also by rearing density of the grandmother. The present results demonstrated that the characteristics of progeny are influenced not only by the crowding conditions experienced by the mother and grandmother but also by the mother's reproductive cycle.     

Is juvenile hormone involved in the maternal regulation of egg size and progeny characteristics in the desert locust?

The role of juvenile hormone (JH) in the maternal regulation of progeny characteristics was examined in the desert locust, Schistocerca gregaria. Female adults of this species are known to produce smaller but more eggs when reared in isolation than do those reared in a group. Eggs laid by isolated females develop green hatchlings typical of solitarious forms, whereas those laid by the latter produce black hatchlings typical of gregarious forms. Topical application of a juvenile hormone analog (JHA), fenoxycarb, or implantation of corpora allata (CA) taken from the migratory locust, Locusta migratoria, caused crowded S. gregaria females to deposit smaller eggs, but did not have a significant effect on the number of eggs per egg pod except at high doses of JHA. The production of smaller eggs by treated and untreated crowded females was closely associated with earlier deposition of the egg pods and shorter oviposition intervals. However, neither JHA application nor CA implantation influenced the progeny characteristics in actively reproducing aged females under crowded conditions, while untreated control females started producing smaller and more eggs upon transfer to isolated conditions. These results may suggest that JH is not directly involved in the maternal regulation of phase-dependent progeny characteristics.     

The role of egg pod foam and rearing conditions of the phase state of the Asian migratory locust Locusta migratoria migratoria (Orthoptera, Acrididae)

Coloration phase state, morphometrical ratios and the numbers of mature oocytes of Locusta migratoria migratoria were examined in a series of experiments to determine the means by which phase characteristics are passed to the next generation. Washing with distilled water of eggs from egg pods laid by gregarious crowd-reared females resulted in solitarization of the hatchlings after their isolation, indicating that a factor present in eggs encapsulated in foam is causal to gregarization. Such locusts showed a significant shift towards the typical solitarious body coloration, morphometry and number of mature oocytes as compared to locusts resulting from unwashed eggs. Gregarious coloration, morphometrical ratios and oocyte numbers could be partially restored when hatchlings from washed eggs were regrouped. When gregarious locusts were reared in isolation, they showed a solitary body color, whereas, morphometry and oocyte numbers were not affected by isolation.     

Adult female desert locusts require contact chemicals and light for progeny gregarization

Crowding causes many organisms to express phenotypic plasticity in various traits. Phase polyphenism in desert locusts represents one extreme example in which a solitary form (solitarious phase) turns into a gregarious form (gregarious phase) in response to crowding. Conspicuous differences in body size and colour occur even in hatchlings. The phase‐specific differences in hatchling characteristics are caused by the tactile stimuli perceived by the antennae of their mother. However, the nature of the tactile stimuli and the mechanism by which the perceived stimuli are processed as a gregarizing signal remain unknown. To explore this problem, the antennae of solitarious adult females of the desert locust Schistocerca gregaria are touched with the bodies of conspecific locusts at different physiological stages and those of other species. The results suggest that a cuticular chemical factor at a specific developmental stage of conspecific locusts causes the solitarious females to produce large eggs that give rise to black hatchlings characteristic of gregarious forms (progeny gregarization), and that this or a similar compound occurs in other acridids, crickets and cockroaches but not in beetles. The involvement of a chemical substance is also supported by hexane extracts of cuticular surfaces of locusts that induce the same effects. Interestingly, crowding induces such gregarizing effects only when the female receives the appropriate stimulus in the presence of light. Solitarious female S. gregaria with their head capsule coated with phosphorescent paint exhibit progeny gregarization in response to crowding and light pulses in darkness, whereas those treated in the same way without light pulses fail to do so.     

Epigenetic transmission of phase in the desert locust, Schistocerca gregaria: Determining the stage sensitive to crowding for the maternal determination of progeny characteristics

Desert locust female adults respond to crowded conditions by changing progeny characteristics such as egg size, clutch size (no. of eggs per pod), hatchling body size and coloration. This study was conducted to determine the stage sensitive to crowding in this locust. Reproductively active females reared in isolation increased egg size and decreased clutch size and the proportion of green hatchlings after exposure to crowded conditions (in which each female was kept with four male adults). These changes depended not only on the timing of exposure to crowded conditions during the reproductive cycle but also on the length of the exposure. By varying the time and length of the exposure, it was found that crowding had no influence on progeny characteristics during the last two days of egg development at 31 °C and that there was a four-day sensitive stage before this period. The sensitive stage coincided with the time when the affected oocytes were 1.5-4 mm long, while the sensitivity to crowding appeared to be constant over the sensitive stage. The larger the magnitude of the increase in egg size after exposure to crowding, the smaller the proportion of green hatchlings (and the larger the proportion of gregarized dark hatchlings); there was a sigmoidal relationship between the two variables. Based on these results, we propose a model for determining the stage sensitive to crowding in both the female parent and the oocytes.     

Phase-specific responses to different qualities of food in the desert locust, Schistocerca gregaria: developmental, morphological and reproductive characteristics

Solitarious female adults are known to produce smaller hatchlings than those produced by gregarious adults of the desert locust, Schistocerca gregaria. This study investigated developmental, morphological and reproductive responses to different qualities of food in hatchlings of different phases. Mortality was higher, the duration of nymphal development longer and adult body weight lighter with a low-quality food than a high-quality food. Gregarious hatchlings showed better survivorship, grew faster and became larger adults than did solitarious ones. The incidence of locusts exhibiting extra molting, which was typically observed in the solitarious phase, was dramatically increased when a low-quality food was given to the solitarious hatchlings. Low-quality food caused locusts to shift morphometric ratios toward the values typical of gregarious forms; smaller F/C (hind femur length/maximum head width) and larger E/F (elytra length/hind femur length). Solitarious hatchlings grown at either high- or low-quality foods and then given high-quality food after adult emergence revealed that food qualities during the nymphal stage influence their progeny quality and quantity via adult body size that influenced reproductive performance. Female adults showed an overshooting response to a shift from low- to high-quality food by increasing egg production that was specific to body size. This study may suggest that gregarious hatchlings are better adapted to adverse food conditions than solitarious counterparts and extra molting is induced even among gregarious hatchlings under poor food conditions.     

The trans-generational phase accumulation in the desert locust: Morphometric changes and extra molting

To understand the underlying trans-generational phase accumulation, a classical morphometric characteristic, the F/C ratio (F, hind femur length; C, maximum head width), of adult desert locusts (Schistocerca gregaria) was monitored over eight consecutive generations. Adult F/C ratios, which are larger in solitarious locusts than in gregarious ones, were negatively correlated to the darkness of body color at hatching. Two successive generations were required for a complete shift from the gregarious (crowd-reared) to the solitarious (isolated-reared) phase and vice versa in the laboratory. That is (1) female adults needed to be exposed to crowded (or isolated) conditions so that their hatchlings would become large (or small) and dark (or green) in color, and (2) the hatchlings then needed to be exposed to crowded (or isolated) conditions for their entire nymphal stage. Solitarious locusts exhibited extra molting that influenced the F/C ratio in the adult stage, but did not exert significant influences on the trans-generational changes in this trait because the incidence was low. The incidence of extra molting was negatively correlated with nymphal survival rates. The morphometric trans-generational changes may be explained without assuming any accumulating internal factor.     

Phase-specific developmental and reproductive strategies in the desert locust

Locusts modify developmental and reproductive traits over successive generations depending on the population density. A trade-off between developmental rate and body size and between progeny size and number is often observed in organisms. In this study, we present evidence that this rule is evaded by desert locusts, Schistocerca gregaria Forsk?l, which often undergo outbreaks. Under isolated conditions, large hatchlings, typical of the gregarious forms, grow faster but emerge as larger adults than do small hatchlings typical of the solitarious forms, except for some individuals of the latter group that undergo extra molting. Under crowded conditions, large and small hatchlings grow at a similar rate, but the former become larger adults than the latter. Small hatchlings show a trade-off between development time and body size at maturation, but this constraint is avoided by large hatchlings. Phase-specific, as well as body size-dependent, differences are also detected in reproductive performance. As adult body size increases, females of a solitarious line produce more but slightly smaller eggs, whereas those of a gregarious line produce more and larger eggs. Total egg mass per pod is larger in gregarious forms than in solitarious forms. A trade-off between egg size and number is shown by a solitarious line but not by a gregarious line that produces relatively large eggs with similar numbers of eggs per pod. These results suggest that phase transformation involves not just a shift of resource allocation but also an enhanced capability expressed in response to crowding.     

Experience pays: offspring survival increases with female age

Life-history theory predicts that, in long-lived organisms, effort towards reproduction will increase with age, and research from oviparous vertebrates largely supports this prediction. In reptiles, where parental care occurs primarily via provisioning of the egg, older females tend to produce larger eggs, which in turn produce larger hatchlings that have increased survival. We conducted an experimental release study and report that maternal age positively influences offspring survivorship in the painted turtle (Chrysemys picta) and predicts offspring survival at least as well as hatchling body size does. These data suggest that, although increasing hatchling size is a major component of reproductive success in older individuals, other factors also contribute.     

Crowded locusts produce hatchlings vulnerable to fungal attack

Transgenerational effects of parental experience on offspring immunity are well documented in the vertebrate literature (where antibodies play an obligatory role), but have only recently been described in invertebrates. We have assessed the impact of parental rearing density upon offspring disease resistance by challenging day-old locust hatchlings (Schistocerca gregaria) from either crowd- or solitary-reared parents with the fungal pathogen Metarhizium anisopliae var. acridum. When immersed in standardized conidia suspensions, hatchlings from gregarious parents suffered greater pathogen-induced mortality than hatchlings from solitary-reared parents. This observation contradicts the basic theory of positive density-dependent prophylaxis and demonstrates that crowding has a transgenerational influence upon locust disease resistance.     

The role of female accessory glands in maternal inheritance of phase in the desert locust Schistocerca gregaria

Accessory glands of crowd-reared females of Schistocerca gregaria were ligatured from the lateral oviducts. Hatchlings resulting from egg pods laid after the treatment showed a significant shift towards solitarious behaviour as compared to hatchlings from control-treated females. Morphometric measurement of hatchlings revealed no consistent difference between ligatured and control females, however, one ratio (hind femur length/vertex width) was approaching significance. Hatchlings from eggs of crowd-reared females behaved solitariously when freshly laid eggs were washed with a saline solution. Gregarious behaviour could be restored when washed eggs were treated with a saline extract of the accessory glands. The colouration of hatchlings was not affected by any treatment. Our findings implicate the accessory glands in the production, release or activation of the recently reported gregarizing factor found in the egg pod foam [McCaffery, A.R., Simpson, S.J., Islam, M.S., Roessingh, P., 1998. A gregarizing factor present in the egg pod foam of the desert locust Schistocerca gregaria. Journal of Experimental Biology 201, 347-363].     

THE EVOLUTION OF MATERNAL INVESTMENT IN LIZARDS: AN EXPERIMENTAL AND COMPARATIVE ANALYSIS OF EGG SIZE AND ITS EFFECTS ON OFFSPRING PERFORMANCE

I used comparative and experimental analysis of egg size in a Sceloporus lizard to examine a fundamental tenet of life-history theory: the presumed trade-offs among offspring number, offspring size, and performance traits related to offspring size that are likely to influence fitness. I analyzed latitudinal and elevational patterns of egg life-history characteristics among populations and experimentally manipulated egg size and hatchling size by removing yolk from the eggs to examine the causal bases of population differences in offspring traits. Mean clutch size among populations increased to the north (seven vs. 12 eggs/clutch, California vs. Washington), whereas egg size decreased (0.65 g vs. 0.40 g). The elevational patterns in southern California paralleled the latitudinal trends. Several offspring life-history traits that are correlated with egg size also varied geographically; these traits included incubation time, hatchling size, growth rate, and hatchling sprint performance. Hatchling viability of experimentally reduced eggs was remarkably high (~70%), even when up to 50% of the yolk was removed. The experimentally reduced eggs and hatchlings demonstrated the degree to which size influences each of the offspring life-history traits considered. Northern eggs hatched sooner, in part because of their small size. Though growth rate is allometrically related to size within each population (i.e., smaller hatchlings grow faster on a mass-specific basis), population differences in growth rate, as measured in the laboratory, are likely to reflect genetic differentiation in the underlying physiology of growth. Moreover, smaller juveniles, because of experimental reduction, had slower sprint speeds than larger juveniles. The slower sprint speed of hatchlings from Washington compared to hatchlings from California is thus largely due to the fact that eggs are smaller in the Washington population. These results provide a basis for interpreting the evolutionary divergence of the suite of traits involved in the evolution of maternal investment per offspring in lizards. For example, evolutionary divergence in some offspring traits functionally related to size (e.g., sprint speed) may be constrained, relative to traits that are determined by other aspects of development or physiology (e.g., growth). I also discuss issues relating to the evolution of maternal investment that could be tested in laboratory and natural populations using experimentally reduced offspring.     

Nonlinear continuum of egg size-number trade-offs in a snake: is egg-size variation fitness related?

The relationship between offspring size and offspring number is crucial to life history evolution. To examine how these two life history variables are coupled and whether an altered balance between them will result in changes in maternal fitness, we manipulated clutch size of the Chinese cobra (Naja atra) by using the techniques of hormonal manipulation and follicle ablation. Females receiving exogenous follicle-stimulating hormone produced more but smaller eggs, and females undergoing follicle ablation produced fewer but larger eggs. Neither body size (body mass and snout-vent length) at hatching nor egg mass at oviposition had a role in determining hatchling survival and growth. Female hatchlings were more likely to die in early post-hatching days and grew more slowly than male hatchlings. Our data show that: (1) there is a nonlinear continuum of egg size-number trade-offs in N. atra within which there is a single inflexion where the rate at which egg size decreases with increasing clutch size, or clutch size increases with decreasing egg size, is maximized; (2) there is a fixed upper limit to egg size for a given-sized female, and the limit is not determined by her body volume; (3) egg size has no role in determining hatchling survival and growth; and (4) the extent to which females may enjoy reproductive benefits in a given reproductive episode depends on how well egg size and egg number are balanced.     

Adaptive difference in daily timing of hatch in two locust species,Schistocerca gregaria and Locusta migratoria: The effects of thermocycles and phase polyphenism

This study examined the effects of temperature and phase polyphenism on egg hatching time in the desert locust, Schistocerca gregaria, and the migratory locust, Locusta migratoria. The two species exhibited differences and similarities in hatching behavior when exposed to different temperature conditions. In 12-h thermocycles of various temperatures, the S. gregaria eggs hatched during the cryoperiod (low temperature period), whereas L. migratoria eggs hatched during the thermoperiod (high temperature period). The eggs of both species hatched during the species-specific period of the thermoperiod in response to a temperature difference as small as 1 °C. Furthermore, the locusts adjusted hatching time to a new thermal environment that occurred shortly before the expected hatching time. In both species, the hatching of the eggs was synchronized to a specific time of the day, and two hatching peaks separated by approximately 1 day were observed at a constant temperature after the eggs were transferred from thermocycles 3 days before hatching. Eggs laid by gregarious females hatched earlier than those laid by solitarious females in S. gregaria but this difference was not observed in L. migratoria.     

孵化水热环境对渔异色蛇孵化卵和孵出幼体的影响

渔异色蛇卵孵化时能从环境中吸收水分导致质量增加,卵质量的增加与初始卵质量和孵化基质湿度有关。较大幅度的孵化基质湿度变化对孵化期、孵化成功率、胚胎动用孵内物质和能量、孵出幼体的性比、大小和质量无显著影响。孵化期随温度升高而缩短,并显示极强的窝间差异。温度对孵出幼体的性别无影响,但显著影响孵化成功率、胚胎对卵内物质和能量的动用、幼体的大小和质量、躯干和剩余卵黄的质量。孵出幼体总长的两性差异不显著,但雌体体长大于雄体而尾长小于雄体。３２℃不适于孵化渔异色蛇卵,该温度下孵出的幼体躯干发育不良,剩余孵黄较多,尾部均呈畸形,孵化过程中能量转化率较低。２４℃和２６℃中孵出的幼体躯干发育良好,孵化过程中能量转化率较高,各项被测定的幼体特征指标均极相似。     

Egg hatching of two locusts,Schistocerca gregaria and Locusta migratoria,in response to light and temperature cycles

The present study showed that the eggs of the desert locust, Schistocerca gregaria, and the migratory locust, Locusta migratoria, responded to photoperiod by hatching when placed on sand in the laboratory. S. gregaria mainly hatched during the dark phase and L. migratoria during the light phase. The importance of light as a hatching cue depended on the magnitude of the temperature change during the thermoperiod; photoperiod played a more important role in the control of hatching time in both species when the magnitude of the temperature change was small. In addition, the eggs of the two species that were covered with sand did not respond to photoperiod and hatched during both the light and dark phases, indicating that light did not penetrate through the sand. Because locust eggs are normally laid as egg pods and a foam plug is deposited between the egg mass and the ground surface, we tested a possibility that naturally deposited eggs perceived light through the foam plug. The eggs that were deposited and left undisturbed in the sand hatched during the light and dark phases at similar frequencies. These results suggest that the eggs of both locust species responded to light and controlled their hatching timing accordingly but would not use light as a hatching cue in the field. The evolutionary significance of the ability of eggs to respond to light in these locusts was discussed.