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.     

Artificial miniaturization causes eggs laid by crowd-reared (gregarious) desert locusts to produce green (solitarious) offspring in the desert locust, Schistocerca gregaria

The mechanism underlying the phase-dependent polyphenism in hatchling body coloration was studied by testing for a possible causal relationship with egg size in the desert locust, Schistocerca gregaria. Crowd-reared (gregarious) females typically produce large, black offspring, whereas females reared in isolation (solitarious) deposit small, green offspring. We first tested for possible genetic differences in the role of egg foam by washing or separating eggs from two strains of locust. No solitarizing effect was found in either of the strains tested, supporting a previous finding, using another laboratory strain, to show that the hatchling body coloration and size are pre-determined in the ovary of the mother and no egg foam factor is involved in the control of the hatchling body coloration. Topical application of fenoxycarb, a juvenile hormone analog (JHA), and implantation of extra corpora allata (CA), taken from Locusta migratoria, caused gregarious female adults of S. gregaria to produce small eggs. Some eggs laid by CA-implanted females produced green hatchlings. All large eggs chosen among those deposited by gregarious females produced black hatchlings. When eggs were either kept on dry filter paper at nearly saturated relative humidity during embryogenesis or pricked with a needle so that some egg yolk was squeezed out, some produced small, green hatchlings. These results suggested that the amount of egg yolk or the availability of yolk material may determine the body coloration of hatchlings.     

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.     

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.     

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.     

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.     

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.     

Maternal investment in reproduction and its consequences in leatherback turtles

Maternal investment in reproduction by oviparous non-avian reptiles is usually limited to pre-ovipositional allocations to the number and size of eggs and clutches, thus making these species good subjects for testing hypotheses of reproductive optimality models. Because leatherback turtles (Dermochelys coriacea) stand out among oviparous amniotes by having the highest clutch frequency and producing the largest mass of eggs per reproductive season, we quantified maternal investment of 146 female leatherbacks over four nesting seasons (2001–2004) and found high inter- and intra-female variation in several reproductive characteristics. Estimated clutch frequency [coefficient of variation (CV) = 31%] and clutch size (CV = 26%) varied more among females than did egg mass (CV = 9%) and hatchling mass (CV = 7%). Moreover, clutch size had an approximately threefold higher effect on clutch mass than did egg mass. These results generally support predictions of reproductive optimality models in which species that lay several, large clutches per reproductive season should exhibit low variation in egg size and instead maximize egg number (clutch frequency and/or size). The number of hatchlings emerging per nest was positively correlated with clutch size, but fraction of eggs in a clutch yielding hatchlings (emergence success) was not correlated with clutch size and varied highly among females. In addition, seasonal fecundity and seasonal hatchling production increased with the frequency and the size of clutches (in order of effect size). Our results demonstrate that female leatherbacks exhibit high phenotypic variation in reproductive traits, possibly in response to environmental variability and/or resulting from genotypic variability within the population. Furthermore, high seasonal and lifetime fecundity of leatherbacks probably reflect compensation for high and unpredictable mortality during early life history stages in this species.     

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.     

两种麻蜥卵和孵出幼体的特征

研究了山地麻蜥和丽斑麻蜥实验条件下的卵及孵出幼体的特征.山地麻蜥产卵雌体的体长大于丽斑麻蜥,窝卵重小于丽斑麻蜥,但平均卵重和相对窝卵重与丽斑麻蜥相似.两种蜥蜴均通过增加卵长径和卵短径来增加卵重,但卵的外形不同,山地麻蜥卵较长.两种蜥蜴卵孵化过程中均吸水增重.相似孵化条件(波动温度、-12 kPa)下,山地麻蜥的孵化期明显比丽斑麻蜥长.山地麻蜥幼体的尾、头部大于丽斑麻蜥,但体重和SVL相似.     

Seasonal shifts in clutch size and egg size in the side-blotched lizard,Uta stansburiana Baird and Girard

Summary There is evidence that the side-blotched lizard, Uta stansburiana, and some other organisms of temperate latitudes produce fewer and larger eggs as the reproductive season progresses. There are at least two models that could explain this phenomenon.Proponents of the parental investment model claim that females are selected to increase egg size, at the cost of clutch size, late in the season in order to produce larger and competitively superior hatchlings at a time when food for hatchlings is in low supply and when juvenile density is high. In this model the selective agent is relative scarcity of food available to hatchlings late in the reproductive season, and the adaptive response is production of larger offspring.The alternative explanation (bet-hedging model) proposed in this paper is based on the view that the amount of food available to females for the production of late-season clutches is unpredictable, and that selection has favored conservatively small clutches in the late season to insure that each egg is at least minimally provisioned. Smaller clutches, which occur most frequently late in the season, are more likely to consist of larger eggs, compared to larger clutches, for two reasons. Firstly, unlike birds, oviparous lizards cannot alter parental investment after their eggs are deposited, and therefore, in cases of fractional optimal clutch size, the next lower integral clutch size is selected with the remaining reproductive energy allocated to increased egg size. With other factors constant, eggs of smaller clutches will increase more in size than eggs of larger clutches when excess energy is divided among the eggs of a clutch. Secondly, unanticipated energy that may become available for reproduction during energy-rich years will similarly increase egg size a greater amount if divided among fewer eggs.     

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.     

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.     

The influence of maternal thermal environments on reproductive traits and hatchling traits in a Lacertid lizard,Takydromus septentrionalis

The thermal environment can induce substantial variation in important life-history traits. Experimental manipulation of the thermal environment can help researchers determine the contribution of this factor to phenotypic variation in life-history traits. During the reproductive season, we kept female northern grass lizards, Takydromus septentrionalis (Lacertidae), in three temperature-controlled rooms (25, 28 and 32 °C) to measure the effect of the maternal thermal environment on reproductive traits. Maternal thermal environment remarkably affected reproductive frequency and thereby seasonal reproductive output, but had little effect on reproductive traits per clutch or hatchling traits. Females kept at 32 °C produced more clutches and thus had shorter clutch intervals than females from 28 to 25 °C. Clutch size, clutch mass, relative clutch mass, egg size and hatchling traits did not vary among the three treatments. The eggs produced by the females were incubated at 27 °C and the traits of hatchlings were measured. The result that egg (offspring) size was independent of maternal thermal environments is consistent with the prediction of the optimal egg size (offspring) theory. The eggs produced by low temperature females (28 and 25 °C) took longer time to complete their post-oviposition development than did eggs produced by high temperature females (32 °C). This suggests that the eggs from low temperatures might have been laid when the embryos were at relatively early stages. Therefore, maternal thermal environment prior to oviposition could affect post-oviposition development in T. septentrionalis.     

Swimming performance of hatchling green turtles is affected by incubation temperature

In an experiment repeated for two separate years, incubation temperature was found to affect the body size and swimming performance of hatchling green turtles (Chelonia mydas). In the first year, hatchlings from eggs incubated at 26°C were larger in size than hatchlings from 28 and 30°C, whilst in the second year hatchlings from 25.5°C were similar in size to hatchings from 30°C. Clutch of origin influenced the size of hatchlings at all incubation temperatures even when differences in egg size were taken into account. In laboratory measurements of swimming performance, in seawater at 28°C, hatchlings from eggs incubated at 25.5 and 26°C had a lower stroke rate frequency and lower force output than hatchlings from 28 and 30°C. These differences appeared to be caused by the muscles of hatchlings from cooler temperatures fatiguing at a faster rate. Clutch of origin did not influence swimming performance. This finding that hatchling males incubated at lower temperature had reduced swimming ability may affect their survival whilst running the gauntlet of predators in shallow near-shore waters, prior to reaching the relative safety of the open sea.     

Parental care and EGG size in salamanders: An examination of the safe harbor hypothesis

The safe harbor hypothesis includes the suggestion that parental care causes the embryonic stage to be the safest harbor, and, therefore, egg size will increase in populations with parental care to decrease the duration of subsequent, higher risk stages. Neither the safe habor hypothesis nor r and K theory seem adequate to explain the correlation between egg size and the presence/absence of parental care among salamanders, a group in which there is a further correlation between the larval (hatchling) habitat and egg size/parental care. Pond-breeding salamanders generally have small eggs and lack parental care, and stream-breeding salamanders generally have large eggs and parental care. I argue that the fundamental difference in the food available to hatchling salamanders between lentic (plankton-rich) and lotic (plankton-poor) environments selects for relatively lower parental investment in the lentic environment. From the standpoint of parental fitness, small (more numerous) hatchlings have a greater payoff where the available food is mall and dense (zooplankton in lentic environments), and large hatchlings are selectively advantageous where the food is of large size and less dense (benthic invertebrates in lotic environments). Selection for larger hatchlings in lotic environments results in longer embryonic periods and, ceteris paribus, greater total embryonic mortality. Embryo hiding and guarding have evolved among lotic-breeding salamanders as compensatory mechanisms to reduce the rate of embryonic mortality. In this view, parental care is a consequence of selection for larger egg size and not an umbrella that allows egg size to increase, contrary to the safe harbor hypothesis. The relationship between variance in parental investment and food available to offspring, developed here for salamanders, may be of general significance. YosiakiItô , a critic of r and K theory, independently arrived at a similar conclusion from a broader data base.     

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.     

The coadaptation of female morphology and offspring size: a comparative analysis in crickets

Few studies of invertebrates have considered combinations of morphological and life history traits in the context of the evolution of reproductive strategies. Cricket species that exploit habitats harsh with respect to egg survival have evolved a long ovipositor, presumably because laying deep in the soil reduces egg mortality. Yet hatchling mortality increases with laying depth, and the ability of hatchlings to climb through the soil increases with egg size. Thus a conflict may exist between survival of the egg and that of the hatchling, inducing a positive covariation between egg size and ovipositor length across species evolving under contrasting selective habitats. We used the phylogenetic autocorrelation method and a path analysis to assess whether egg size coevolved with ovipositor length across 40 species of crickets, and whether egg size was affected by body size or ecological factors that influence egg mortality. Body size and ovipositor length were affected by taxonomic association, whereas common ancestry had no significant effect on egg size, diapausing strategy, and oviposition preference for soil types. The path model indicated that 29.11% of the variance in egg size was explained by independent evolution. As expected, ovipositor length was positively correlated with egg size, and species diapausing in the egg stage produced larger eggs than crickets diapausing in the nymphal stage or with no diapause. Ovipositor length and diapausing strategy were the first and second most important traits, respectively, in term of the proportion of variance in egg size explained by specific values. These results support the hypothesis that the ability of hatchlings to climb through the soil, and variation in diapause strategies, are general selective factors affecting the evolution of egg size in crickets. Phylogeny explained 51.01% of the variance in egg size. Egg size in a current cricket species, however, was not directly determined by egg size in its ancestor. Instead, it was strongly related to the phylogenetic values of body size and ovipositor length. Such indirect phylogenetic effects of body size and ovipositor length may have arisen because clades originating from ancestors with different ovipositor lengths experienced different selective pressures on egg size. Recelived: 13 October 1995 / Accepted: 30 September 1996     

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].     

Quantity or quality? Determinants of maternal reproductive success in tropical pythons (Liasis fuscus)

A female''s reproductive output (size and number of offspring) may say little about her reproductive success; the ''quality'' of her progeny and the time that they are produced may be more important in this respect. We marked and released 1224 hatchling water pythons (Liasis fuscus) from 116 clutches of laboratory-incubated eggs, in a study site in tropical Australia. Clutches varied widely in the number of eggs, mean offspring sizes, the proportion of eggs that hatched, and recapture rates of offspring. Clutch size was not significantly correlated with the number of recaptured hatchlings in either year, nor was mean offspring size related to recapture probability. Instead, offspring recapture rates varied as a function of the time of hatching. Recapture rates were higher for hatchlings released in a year with high prey availability than in a year with few prey. In addition, recapture rates were higher for earlier-hatching clutches in the year with few prey. The other significant effect on recapture rates involved offspring viability: some clutches had a much higher proportion of surviving offspring than did others, and recapture rates were higher from clutches with higher hatching success (i.e. proportion of eggs hatching). Hence, the usual measures of reproductive output (clutch size and offspring size) offer only a poor index of a female''s reproductive success in this system.