Effects of hatchling body colour and rearing density on body colouration in last-stadium nymphs of the desert locust, Schistocerca gregaria

Abstract.  The influences of hatchling character and rearing density on body colour at the last-nymphal stadium are investigated for the desert locust, Schistocerca gregaria . Hatchlings are divided into five groups based on the darkness of the body colour and reared either under isolated or crowded conditions. Two types of body colour variation at the last-nymphal stadium are separately analysed (i.e. the background colour and black patterns). Under isolated conditions, the background body colour is either greenish or brownish. Most individuals are greenish and the highest percentage of brownish insects is obtained from hatchlings with the darkest body colour. Under crowded conditions, the background colour is yellow or orange and the percentage of yellowish nymphs tends to decrease when they are darker at hatching. The intensity of black patterns differs depending on the body colour at hatching and subsequent rearing density. Most isolated-reared nymphs exhibit few or no black patterns but nymphs with some black patterns also appear, particularly among those that had been dark at hatching. Under crowded conditions, the black patterns become more intense when they are darker at hatching. Therefore, last-stadium nymphs with typical solitarious or gregarious body colouration appear when they have the phase-specific body colouration at hatching as well. The present results demonstrate that both body colour at hatching and rearing density during nymphal development influence body colouration at the last-nymphal stadium.     

A behavioural analysis of phase change in the desert locust

A programme of research into phase change in the desert locust, Schistocerca gregaria, is described. The ability to change phase between solitarious and gregarious forms in response to population density is a key feature of locusts and is central to their occasional yet catastrophic impact on humans. Phase polymorphism is an extreme form of phenotypic plasticity. The most labile phase characteristic is behaviour. It is argued that a fully integrated study of behavioural phase change provides a powerful tool for understanding both the mechanisms of phase change and locust population dynamics, both of which offer possibilities for improved management and control of desert locust plagues. An assay for measuring behavioural phase-state in individual locusts was derived, based on logistic regression analysis. Experiments are described that used the assay to quantify the time-course of behavioural change, both within the life of individual locusts and across generations. The locust-related stimuli that provoke behavioural gregarization were investigated. Complex interactions were found between tactile, visual and olfactory stimuli, with the former exerting the strongest effect. Behavioural analysis also directed a study of the mechanisms whereby adult females exert an epigenetic influence over the phase-state of their developing offspring. Female locusts use their experience of the extent and recency of being crowded to predict the probability that their offspring will emerge into a high-density population, and alter the development of their embryos accordingly through a gregarizing agent added to the foam that surrounds the eggs at laying. There is also a less pronounced paternal influence on hatchling phase-state. An understanding of the time-course of behavioural phase change led to a study of the effect of the fine-scale distribution of resources in the environment on interactions between individual locusts, and hence on phase change. This, in turn, stimulated an exploration of the implications of individual behavioural phase change for population dynamics. Cellular automata models were derived that explore the relationships between population density, density of food resources and the distribution of resources in the environment. The results of the simulation showed how the extent of gregarization within a population increases with rising population size relative to food abundance and increasing concentration of food resources. Of particular interest was the emergence of critical zones across particular combinations of resource abundance, resource distribution and population size, where a solitarious population would rapidly gregarize. The model provided the basis for further laboratory and field experiments, which are described.     

Density-dependent accumulation of phase characteristics in a natural population of the desert locust Schistocerca gregaria

Abstract. Phase characteristics of locusts from parents that experienced different population densities were investigated under field conditions in Morocco. The density experienced by adults induced a marked phase change in colour, behaviour and morphometry of their offspring. A high-density subpopulation gave rise to a preponderance of black hatchlings that exhibited a high level of aggregation as later stage nymphs and showed gregarious morphometric features as adults, whereas a low-density subpopulation produced a majority of green hatchlings with a lesser tendency to group as final-instar nymphs and more solitarious morphometry as adults. The constrained isolation of insects from the low-density subpopulation, or crowding of insects from the high-density subpopulation, resulted in a behavioural and morphometric change towards even more solitarious characteristics in the former and more pronounced gregarious characteristics in the latter, relative to field-caught insects of the same age. These results from the field are consistent with those in the laboratory and provide more evidence for the dual roles of an individual locust's experience of crowding as well as that of its parents in density-dependent phase change.     

Morphological and behavioural characteristics of a gynandromorph of the desert locust, Schistocerca gregaria

Abstract.  Morphological and behavioural characteristics are investigated for a gynandromorph of the desert locust, Schistocerca gregaria , appearing under isolated rearing conditions in the laboratory. It has both male and female external reproductive organs bilaterally. The body size and dimensions are similar to a normal male. Morphometric traits (fore wing length/maximum head width ratio and fore wing length/hind femur length ratio) of the gynandromorph are typical for the values of solitarious locusts. When the gynandromorph is placed into an arena holding ten sexually mature gregarious females, it shows a distinct male behaviour: it jumps on a female and tries to mate with her. When kept together with males, males recognize this gynandromorph as a female because some of them try to mount, although no successful copulation is observed. The results suggest that the gynandromorph might have had a female-specific pheromone. Dissection reveals that the gynandromorph has no testis but abnormal ovaries containing vitellogenic oocytes. These observations indicate that the gynandromorph obtained has a mixture of male and female morphological characteristics and behaves like a male but is recognized as a female by conspecific males.     

When mother knows best: A population genetic model of transgenerational versus intragenerational plasticity

Many organisms exhibit phenotypic plasticity; producing alternate phenotypes depending on the environment. Individuals can be plastic (intragenerational or direct plasticity), wherein individuals of the same genotype produce different phenotypes in response to the environments they experience. Alternatively, an individual's phenotype may be under the control of its parents, usually the mother (transgenerational or indirect plasticity), so that mother's genotype determines the phenotype produced by a given genotype of her offspring. Under what conditions does plasticity evolve to have intragenerational as opposed to transgenerational genetic control? To explore this question, we present a population genetic model for the evolution of transgenerational and intragenerational plasticity. We hypothesize that the capacity for plasticity incurs a fitness cost, which is borne either by the individual developing the plastic phenotype or by its mother. We also hypothesize that individuals are imperfect predictors of future environments and their capacity for plasticity can lead them occasionally to make a low‐fitness phenotype for a particular environment. When the cost, benefit and error parameters are equal, we show that there is no evolutionary advantage to intragenerational over transgenerational plasticity, although the rate of evolution of transgenerational plasticity is half the rate for intragenerational plasticity, as predicted by theory on indirect genetic effects. We find that transgenerational plasticity evolves when mothers are better predictors of future environments than offspring or when the fitness cost of the capacity for plasticity is more readily borne by a mother than by her developing offspring. We discuss different natural systems with either direct intragenerational plasticity or indirect transgenerational plasticity and find a pattern qualitatively in accord with the predictions of our model.     

Error management theory and the adaptive significance of transgenerational maternal‐stress effects on offspring phenotype

It is well established that circulating maternal stress hormones (glucocorticoids, GCs) can alter offspring phenotype. There is also a growing body of empirical work, within ecology and evolution, indicating that maternal GCs link the environment experienced by the mother during gestation with changes in offspring phenotype. These changes are considered to be adaptive if the maternal environment matches the offspring's environment and maladaptive if it does not. While these ideas are conceptually sound, we lack a testable framework that can be used to investigate the fitness costs and benefits of altered offspring phenotypes across relevant future environments. We present error management theory as the foundation for a framework that can be used to assess the adaptive potential of maternal stress hormones on offspring phenotype across relevant postnatal scenarios. To encourage rigorous testing of our framework, we provide field‐testable hypotheses regarding the potential adaptive role of maternal stress across a diverse array of taxa and life histories, as well as suggestions regarding how our framework might provide insight into past, present, and future research. This perspective provides an informed lens through which to design and interpret experiments on the effects of maternal stress, provides a framework for predicting and testing variation in maternal stress across and within taxa, and also highlights how rapid environmental change that induces maternal stress may lead to evolutionary traps.     

Non‐additive effects of simulated heat waves and predators on prey phenotype and transgenerational phenotypic plasticity

Understanding the effects of extreme climatic events on species and their interactions is of paramount importance for predicting and mitigating the impacts of climate change on communities and ecosystems. However, the joint effects of extreme climatic events and species interactions on the behaviour and phenotype of organisms remain poorly understood, leaving a substantial gap in our knowledge on the impacts of climatic change on ecological communities. Using an aphid–ladybeetle system, we experimentally investigated the effects of predators and heat shocks on prey body size, microhabitat use, and transgenerational phenotypic plasticity (i.e., the asexual production of winged offspring by unwinged mothers). We found that (i) aphids were smaller in the presence of predators but larger when exposed to frequent heat shocks; (ii) frequent heat shocks shifted aphid distribution towards the plant's apex, but the presence of predators had the opposite effect and dampened the heat‐shock effects; and (iii) aphids responded to predators by producing winged offspring, but heat shocks strongly inhibited this transgenerational response to predation. Overall, our experimental results show that heat shocks inhibit phenotypic and behavioural responses to predation (and vice versa) and that such changes may alter trophic interactions, and have important consequences on the dynamics and stability of ecological communities. We conclude that the effects of extreme climatic events on the phenotype and behaviour of interacting species should be considered to understand the effects of climate change on species interactions and communities.     

Small-scale vegetation patterns in the parental environment influence the phase state of hatchlings of the desert locust

Desert locusts (Schistocerca gregaria Forskål (Orthoptera: Acrididae)) change phase in response to population density. Solitarious insects avoid one another; when crowded, they shift to the gregarious phase and aggregate. Laboratory experiments and individual‐based modelling have shown that small‐scale resource distribution can affect locust phase state via an influence on crowding. Laboratory work has also shown that parental phase state is transmitted to offspring via maternal inheritance. These effects had not been investigated in the field previously. We maintained small populations of adult desert locusts in semi‐field enclosures with different distribution patterns of a single plant species (Hyoscyamus muticus L. (Solanaceae)). The offspring of locusts exposed to more clumped patterns of vegetation exhibited more gregarious behaviour when tested in a behavioural phase assay than did progeny from parents left in enclosures with more scattered vegetation. These effects on nymphal behaviour appeared to be mediated by influences of resource distribution on adult phase state. Phase state in small semi‐field populations was influenced by small‐scale vegetation distribution. Phase differences engendered by environmental structure were maintained in time and transmitted to progeny.     

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.     

Virulence of Metarhizium anisopliae and Beauveria bassiana isolates and the effects of fungal infection on the reproduction potential of Rhiphicephalus microplus engorged females

The aim of the study was to assess the virulence of five Metarhizium anisopliae (Ma) and three of Beauveria bassiana (Bb) isolates, and the effect of the fungal infection to the reproduction of engorged females from two colonies of Rhiphicephalus microplus; one colony was collected from naturally infested cattle (Native) and the other one from a laboratory colony (Media Joya). Virulence was evaluated using the immersion technique at a concentration of 1?×?10⁸ conidia/ml; control groups received a water suspension with Tween 80 (0.1%). The Reproductive Efficiency Index ‘REI’ (eggs laid/engorged female weight) and the Reproductive Aptitude Index ‘RAI’ (eggs hatched as larvae/engorged female weight) were calculated for both groups. This experiment shows that two entomopathogenic fungal isolates, Bb115 and Ma136, caused high mortality from 5 days post-treatment (PT), reaching mortality rates of 99–100% at 15 days PT in both R. microplus colonies. The Bb115 isolate caused 98 and 79% reduction in egg oviposition in the field and laboratory colonies, respectively, while the reduction in egg hatchability was 98 and 89% in the field and laboratories colonies, respectively. In the case of Ma136, the egg oviposition was reduced in 73% in the field colony and 64% in laboratory colony, while in the field and laboratory colonies, with a reduction in egg hatchability of 73% and 86%, respectively. These results indicate the potential of Bb115 and Ma136 isolates as possible biological control agents of R. microplus.     

Unique maternal and environmental effects on the body morphology of the Least Killifish,Heterandria formosa

An important step in diagnosing local adaptation is the demonstration that phenotypic variation among populations is at least in part genetically based. To do this, many methods experimentally minimize the environmental effect on the phenotype to elucidate the genetic effect. Minimizing the environmental effect often includes reducing possible environmental maternal effects. However, maternal effects can be an important factor in patterns of local adaptation as well as adaptive plasticity. Here, we report the results of an experiment with males from two populations of the poeciliid fish, Heterandria formosa, designed to examine the relative influence of environmental maternal effects and environmental effects experienced during growth and development on body morphology, and, in addition, whether the balance among those effects is unique to each population. We used a factorial design that varied thermal environment and water chemistry experienced by mothers and thermal environment and water chemistry experienced by offspring. We found substantial differences between the two populations in their maternal and offspring norms of reaction of male body morphology to differences in thermal environment and water chemistry. We also found that the balance between maternal effects and postparturition environmental effects differed from one thermal regime to another and among traits. These results indicate that environmental maternal effects can be decidedly population‐specific and, as a result, might either contribute to the appearance of or blur evidence for local adaptation. These results also suggest that local adaptation might also occur through the evolution of maternal norms of reaction to important, and varying, environmental factors.     

The influence of environmental microstructure on the behavioural phase state and distribution of the desert locust Schistocerca gregaria

Abstract. In previous studies we used logistic regression analysis to quantify the change in behavioural phase state of Schistocerca gregaria (Forskål) nymphs subjected to variations in population density. Such work involved restricting insects in small containers either alone or in a crowd. In the present paper we have shown that the fine-scale distribution of food plants, perches and favourable microclimatic sites influences the spatial distribution of locusts, both in the laboratory and under semi-field conditions. When multiple resource sites were provided, solitarious locusts tended to disperse and behavioural gregarization was inhibited. However, provision of only a single site promoted congregation, overcoming the tendency of solitarious insects to avoid each other, and led to behavioural gregarization. The time-course and extent of this response was fully consistent with our earlier experiments using enforced crowding. We suggest that such quantitative, experimental studies of the effects of environmental microstructure on behaviour may yield fundamental insights into the dynamics of plague formation in the desert locust.     

Lethal effects of Gliocladium virens,Beauveria bassiana and Metarhizium anisopliae on the malaria vector Anopheles albimanus (Diptera: Culicidae)

Control of Anopheles albimanus, the main vector of malaria on the coast of the State of Chiapas, is based mainly on application of chemical insecticides, which has resulted in resistance to most registered insecticides. Strategies for biological control may provide sustainable alternatives. We report on the lethal effects of a native isolate of Gliocladium virens on An. albimanus larvae and adults, compared to that of strains of Beauveria bassiana and Metarhizium anisopliae. Conidial suspensions of G. virens, B. bassiana and M. anisopliae cultured on Sabouraud agar were tested in bioassays with An. albimanus larvae and adults. Mosquito larvae were more susceptible to all fungi, compared to adults. On early and late instar larvae, M. anisopliae showed the most pathogenic effect (LC₅₀ of 1.4×10⁵ conidia/mL in early instars; 1.1×10⁵ conidia/mL in late instars), followed by G. virens (LC₅₀ of 3.3×10⁵ conidia/mL in early instars and 3.5×10⁶ conidia/mL in late instars). Metarhizium anisopliae sensu lato and the native G. virens could be considered good choices for An. albimanus control in southern Mexico.     

The inhibitory effect of the fungal toxin, destruxin A, on behavioural fever in the desert locust

During an infection locusts behaviourally fever by seeking out higher environmental temperatures. This behaviour places the pathogen at sub-optimal growth temperatures while improving the efficiency of the immune system, thereby prolonging the lifespan of the host. It is therefore in the interest of the pathogen to either adapt to fever-like temperatures or to evolve mechanisms to interfere with, or inhibit fever. We investigated the behavioural fever response of desert locusts to two fungal pathogens. A prolonged fever was observed in locusts infected with Metarhizium acridum. However, fever was comparatively short-lived during infection with Metarhizium robertsii. In both cases restriction of thermoregulation reduced lifespan. Destruxin A (dtx A) produced by M. robertsii, but not M. acridum has previously been associated with the inhibition of the insect immune system. Injection of dtx A during infection with the fever-causing M. acridum inhibited fever and was particularly effective when administered early on in infection. Furthermore, locusts injected with dtx A were more susceptible to M. acridum infection. Therefore engineering M. acridum isolates currently used for locust biocontrol, to express dtx A may improve efficiency of control by interfering with fever.     

Genetic and maternal influences on life history plasticity in milkweed bugs (Oncopeltus): response to temperature

This study was designed to examine life history flexibility arising from phenotypic plasticity in response to temperature and from maternal effects in response to reproductive diapause in a temperate zone population of the milkweek bug (Oncopeltus fasciatus). We employed a split-family, first-cousin, full-sib design with siblings reared at different temperatures in order to quantify phenotypic plasticity, maternal effects, and variation for each. The following traits were analyzed: development time, age at first reproduction, longevity, early-life fecundity, and wing length. We found both life history plasticity and maternal effects on life history traits which tend to enhance the colonizing ability of offspring born to mothers that have undergone reproductive diapause. We were unable to demonstrate additive genetic variation for plasticity for any of the traits, while for development time and wing length we found variation due to non-additive genetic or common-environmental sources. We were also unable to demonstrate additive genetic variation for maternal effects, although variation may exist at low levels that are difficult to detect using cousin-families. The apparent lack of variation in this population would constrain evolution of life history flexibility even though considerable flexibility exists in the phenotype.     

The evolutionary ecology of seed germination of Arabidopsis thaliana: variable natural selection on germination timing

Germination timing of Arabidopsis thaliana displays strong plasticity to geographic location and seasonal conditions experienced by seeds. We identified which plastic responses were adaptive using recombinant inbred lines in a field manipulation of geographic location (Kentucky, KY; Rhode Island, RI), maternal photoperiod (14-h and 10-h days), and season of dispersal (June and November). Transgressive segregation created novel genotypes that had either higher fitness or lower fitness in certain environments than either parent. Natural selection on germination timing and its variation explained 72% of the variance in fitness among genotypes in KY, 30% in June-dispersed seeds in RI, but only 4% in November-dispersed seeds in RI. Therefore, natural selection on germination timing is an extremely efficient sieve that can determine which genotypes can persist in some locations, and its efficiency is geographically variable and depends on other aspects of life history. We found no evidence for adaptive responses to maternal photoperiod during seed maturation. We did find adaptive plasticity to season of seed dispersal in RI. Seeds dispersed in June postponed germination, which was adaptive, while seeds dispersed in November accelerated germination, which was also adaptive. We also found maladaptive plasticity to geographic location for seeds dispersed in June, such that seeds dispersed in KY germinated much sooner than the optimum time. Consequently, bet hedging in germination timing was favorable in KY; genotypes with more variation in germination timing had higher fitness because greater variation was associated with postponed germination. Selection on germination timing varied across geographic location, indicating that germination timing can be a critical stage in the establishment of genotypes in new locations. The rate of evolution of germination timing may therefore strongly influence the rate at which species can expand their range.     

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.     

Resporulation of Metarhizium anisopliae granules on soil and mortality of Tenebrio molitor: Implications for wireworm management in sweetpotato

In Australia, sweetpotato (Ipomoea batatas L.) is vulnerable to root feeding insect pests such as wireworms (e.g., Agrypnus spp.). The number of registered insecticides to control these insect pests is limited and often pest pressure, for example by wireworms, is severe close to harvest, further limiting what insecticides can be applied. Incorporating biological control agents such as entomopathogenic fungi (e.g., Metarhizium anisopliae) into integrated pest management programmes may be feasible in sweetpotato. M. anisopliae has been shown to be effective in controlling more than 200 insects and it is able to reside and grow in the rhizosphere and rhizoplane, suggesting that M. anisopliae could be a promising candidate against soil insect pests. In the study presented here, M. anisopliae was formulated into calcium alginate granules fortified with nutrients. The resporulation of the fungal granules was tested on four different soil types in the laboratory. The biocontrol efficacy of the resulting fungal growth was also examined using larval mealworms, Tenebrio molitor as a model insect in the laboratory and the glasshouse. Our results indicated that sterilised soil favoured optimal fungal resporulation, although different soil types did not have a significant effect on fungal resporulation. The resulting fungal resporulation and growth on sterilised soil caused high mortality (up to 76%) of larval mealworms in the glasshouse, whereas the fungal granules applied to non-sterile soil demonstrated poor resporulation that led to low mortality (13%) of larval mealworms. The result of this study indicates that the manipulation of microbial populations in field soil is required to enhance the fungal growth and potential insect control against wireworms in the field.