Towards a mechanistic understanding of insect life history evolution: oxygen‐dependent induction of moulting explains moulting sizes

Moults characterise insect growth trajectories, typically following a consistent pattern known as Dyar's rule; proportional size increments remain constant across inter‐instar moults. Empirical work suggests that oxygen limitation triggers moulting. The insect respiratory system, and its oxygen supply capacity, grows primarily at moults. It is hypothesized that the oxygen demand increases with increasing body mass, eventually meeting the oxygen supply capacity at an instar‐specific critical mass where moulting is triggered. Deriving from this hypothesis, we develop a novel mathematical model for moulting and growth in insect larvae. Our mechanistic model has great success in predicting moulting sizes in four butterfly species, indirectly supporting a size‐dependent mechanism underlying moulting. The results demonstrate that an oxygen‐dependent induction of moulting mechanism would be sufficient to explain moulting sizes in the study species. Model predictions deviated slightly from Dyar's rule, the deviations being typically negligible within the present data range. The developmental decisions (e.g. moulting) made by growing larvae significantly affect age and size at maturity, which has important life history implications. The successful modelling of moulting presented here provides a novel framework for the development of realistic insect growth models, which are required for a better understanding of life history evolution.     

Cannibalism of parasitoid‐attacked conspecifics in a non‐carnivorous caterpillar

Cannibalism, the killing and consumption of conspecifics, can even occur in insect species typically considered to be non‐carnivorous. Of particular interest is the cannibalism of parasitoid‐attacked conspecifics, which could reduce parasitism levels in subsequent generations for that conspecific population. This study reports on the occurrence and some of the consequences of cannibalism in parasitoid‐attacked obliquebanded leafroller, Choristoneura rosaceana (Harris) (Lepidoptera: Tortricidae). We show that larvae of C. rosaceana, which is considered to be an herbivorous caterpillar species, did not prey upon live conspecifics, but readily consumed conspecifics attacked by Habrobracon gelechiae Ashmead (Hymenoptera: Braconidae). Further examination found that C. rosaceana larvae feeding on parasitoid‐attacked conspecifics, since their fourth instar, suffered a higher mortality and reduction in body size than those fed on plant material only. The cannibalism of attacked conspecifics did not appear to offer any nutrient benefits for the cannibal. To our best knowledge, this is the first empirical example of the occurrence and some of the consequences of cannibalism by a non‐carnivorous insect on its parasitoid‐attacked conspecifics. We discuss the adaptive significance of such cannibalism on parasitoid‐attacked conspecifics with respect to a trans‐generational fitness gain for the population through the killing of the parasitoids, thereby reducing parasitism in subsequent generations.     

Making a queen: an epigenetic analysis of the robustness of the honeybee (Apis mellifera) queen developmental pathway

Specialized castes are considered a key reason for the evolutionary and ecological success of the social insect lifestyle. The most essential caste distinction is between the fertile queen and the sterile workers. Honeybee (Apis mellifera) workers and queens are not genetically distinct, rather these different phenotypes are the result of epigenetically regulated divergent developmental pathways. This is an important phenomenon in understanding the evolution of social insect societies. Here, we studied the genomic regulation of the worker and queen developmental pathways, and the robustness of the pathways by transplanting eggs or young larvae to queen cells. Queens could be successfully reared from worker larvae transplanted up to 3 days age, but queens reared from older worker larvae had decreased queen body size and weight compared with queens from transplanted eggs. Gene expression analysis showed that queens raised from worker larvae differed from queens raised from eggs in the expression of genes involved in the immune system, caste differentiation, body development and longevity. DNA methylation levels were also higher in 3‐day‐old queen larvae raised from worker larvae compared with that raised from transplanted eggs identifying a possible mechanism stabilizing the two developmental paths. We propose that environmental (nutrition and space) changes induced by the commercial rearing practice result in a suboptimal queen phenotype via epigenetic processes, which may potentially contribute to the evolution of queen–worker dimorphism. This also has potentially contributed to the global increase in honeybee colony failure rates.     

A gene‐driven recovery mechanism: Drosophila larvae increase feeding activity for post‐stress weight recovery

Recovery from weight loss after stress is important for all organisms, although the recovery mechanisms are not fully understood. We are working to clarify these mechanisms. Here, we recorded enhanced feeding activity of Drosophila melanogaster larvae from 2 to 4 h after heat stress at 35°C for 1 h. During the post‐stress period, expression levels of sweet taste gustatory receptor genes (Grs), Gr5a, Gr43a, Gr64a, and Gr64f, were elevated, whereas bitter taste Grs, Gr66a, and Gr33a, were decreased in expression and expression of a non‐typical taste receptor Gr, Gr68a, was unchanged. Similar upregulation of Gr5a and downregulation of Gr66a was recorded after cold stress at 4°C. Expression levels of tropomyosin and ATP synthase ß subunit were significantly increased in larval mouth parts around 3 to 5 h after the heat stress. We infer that up‐regulation of post‐stress larval feeding activity, and weight recovery, is mediated by increasing capacity for mouth part muscular movements and changes in taste sensing physiology. We propose that Drosophila larvae, and likely insects generally, express an efficient mechanism to recover from weight loss during post‐stress periods.     

Predator‐induced spine length and exocuticle thickness in Leucorrhinia dubia (Insecta: Odonata): a simple physiological trade‐off?

1. Morphological defence structures evolve against predators but are costly to the individual, and are induced only when required. A well‐studied example is the development of longer abdominal spines in dragonfly larvae in the presence of fish. Numerous attempts to discover trade‐offs between spine size and behaviour, development time or body size have, however, produced little evidence. 2. We considered a physiological trade‐off. Spines consist of cuticle and using material to build longer structures may result in less material remaining elsewhere. We therefore measured exocuticle thickness at nine locations on Leucorrhinia dubia larvae from habitats with and without fish. 3. Our results show a significant effect of the interaction between fish presence and spine length on head and fore leg exocuticle thickness. Relative thickness increased with relative length of lateral spine 9 in the absence of fish, whereas no such relationship existed with fish. Hence, synthesis and secretion of cuticle material occur as a trade‐off when larvae react to fish presence. 4. We assume the mechanism to be a selective synthesis of material with different responses in different parts of the larval body. These findings offer a new angle to the fish/spine trade off debate.     

Catchment context and the bottom‐up regulation of the abundance of specialist semi‐aquatic weevils on water hyacinth

1. Bottom‐up regulation is prevalent in plant–herbivore interactions and is thought to be particularly important in the case of aquatic plants and their specialist insect herbivores. 2. Recently published mesocosm studies have shown that the abundance of specialist Neochetina weevils, N. bruchi and N. eichhorniae, on water hyacinth (Eichhornia crassipes) are principally under the influence of nutrients in plant tissues. 3. We examined historical patterns of the abundance of these species of semi‐aquatic weevils in two water bodies from catchments with significantly different nutrient loads in subtropical Australia to test the validity of the published conceptual model of bottom‐up regulation. 4. Our results revealed that these weevils are indeed under bottom‐up regulation under field conditions. However, the nature of this regulation appears to be influenced by the broader catchment context of the water hyacinth‐infested water body, with plant tissue nutrients influencing weevil abundance more in the catchment with lower nutrient run‐offs. 5. Our findings reaffirm the importance of bottom‐up regulation in plant–insect interactions, add to the growing evidence of indirect effects spanning terrestrial and aquatic ecosystems, and inform management of water hyacinth using these weevils as biocontrol agents.     

Imaginal discs regulate developmental timing in Drosophila melanogaster

The regulation of body size in animals involves mechanisms that terminate growth. In holometabolous insects growth ends at the onset of metamorphosis and is contingent on their reaching a critical size in the final larval instar. Despite the importance of critical size in regulating final body size, the developmental mechanisms regulating critical size are poorly understood. Here we demonstrate that the developing adult organs, called imaginal discs, are a regulator of critical size in larval Drosophila. We show that damage to, or slow growth of, the imaginal discs is sufficient to retard metamorphosis both by increasing critical size and extending the period between attainment of critical size and metamorphosis. Nevertheless, larvae with damaged and slow growing discs metamorphose at the same size as wild-type larvae. In contrast, complete removal of all imaginal tissue has no effect on critical size. These data indicate that both attainment of critical size and the timely onset of metamorphosis are regulated by the imaginal discs in Drosophila, and suggest that the termination of growth is coordinated among growing tissues to ensure that all organs attain a characteristic final size.     

Life history evolution and cellular mechanisms associated with increased size in high‐altitude Drosophila

Understanding the physiological and genetic basis of growth and body size variation has wide‐ranging implications, from cancer and metabolic disease to the genetics of complex traits. We examined the evolution of body and wing size in high‐altitude Drosophila melanogaster from Ethiopia, flies with larger size than any previously known population. Specifically, we sought to identify life history characteristics and cellular mechanisms that may have facilitated size evolution. We found that the large‐bodied Ethiopian flies laid significantly fewer but larger eggs relative to lowland, smaller‐bodied Zambian flies. The highland flies were found to achieve larger size in a similar developmental period, potentially aided by a reproductive strategy favoring greater provisioning of fewer offspring. At the cellular level, cell proliferation was a strong contributor to wing size evolution, but both thorax and wing size increases involved important changes in cell size. Nuclear size measurements were consistent with elevated somatic ploidy as an important mechanism of body size evolution. We discuss the significance of these results for the genetic basis of evolutionary changes in body and wing size in Ethiopian D. melanogaster.     

Medicago truncatula-derived calcium oxalate crystals have a negative impact on chewing insect performance via their physical properties

Plant structural traits often act as defenses against herbivorous insects, causing them to avoid feeding on a given plant or tissue. Mineral crystals of calcium oxalate in Medicago truncatula Gaertn. (Fabaceae) leaves have previously been shown to be effective deterrents of lepidopteran insect feeding. They are also inhibitors of conversion of plant material into insect body mass during or after consumption. Growth of beet armyworm, Spodoptera exigua Hübner (Lepidoptera: Noctuidae), larvae was correspondingly greater on calcium oxalate‐defective (cod) mutants of M. truncatula with lower levels of crystal accumulation. Data presented here show that insects feeding on M. truncatula leaves with calcium oxalate crystals experience greater negative effects on growth and mandible wear than those feeding on artificial diet amended with smaller amorphous crystals from commercial preparations. Commercial calcium oxalate can be added to insect artificial diet at levels up to 7.5‐fold higher than levels found in wild‐type M. truncatula leaves with minimal effect on insect growth or lepidopteran mandibles. These data suggest that negative impacts of calcium oxalate in the diet of larvae are due to physical factors, and not toxicity of the compound, as high levels of the commercial crystals are readily tolerated. In contrast to the dramatic physical effects that M. truncatula‐derived crystals have on insect mandibles, we could detect no damage to insect peritrophic gut membranes due to consumption of these crystals. Taken together, the data indicate that the size and shape of prismatic M. truncatula oxalate crystals are important factors in determining effects on insect growth. If manipulation of calcium oxalate is to be used in developing improved insect resistance in plants, then our findings suggest that controlling not only the overall amount, but also the size and shape of crystals, could be valuable traits in selecting desirable plant lines.     

Life histories of closely related amphidromous and non‐migratory fish species: a trade‐off between egg size and fecundity

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Increased temperature reduces herbivore host‐plant quality

Globally increasing temperatures may strongly affect insect herbivore performance, as their growth and development is directly linked to ambient temperature as well as host‐plant quality. In contrast to direct effects of temperature on herbivores, indirect effects mediated via thermal effects on host‐plant quality are only poorly understood, despite having the potential to substantially impact performance and thereby to alter responses to the changing climatic conditions. We here use a full‐factorial design to explore the direct (larvae were reared at 17 °C or 25 °C) and indirect effects (host plants were reared at 17 °C or 25 °C) of temperature on larval growth and life‐history traits in the temperate‐zone butterfly Pieris napi. Direct temperature effects reflected the common pattern of prolonged development and increased body mass at lower temperatures. At the higher temperature, efficiency of converting food into body matter was much reduced being accompanied by an increased food intake, suggesting compensatory feeding. Indirect temperature effects were apparent as reduced body mass, longer development time, an increased food intake, and a reduced efficiency of converting food into body matter in larvae feeding on plants grown at the higher temperature, thus indicating poor host‐plant quality. The effects of host‐plant quality were more pronounced at the higher temperature, at which compensatory feeding was much less efficient. Our results highlight that temperature‐mediated changes in host‐plant quality are a significant, but largely overlooked source of variation in herbivore performance. Such effects may exaggerate negative effects of global warming, which should be considered when trying to forecast species' responses to climate change.     

Body size regulation by maturation steroid hormones: a <Emphasis Type="Italic">Drosophila</Emphasis> perspective

The mechanism that determines the specific body size of an animal is a fundamental biological question that remains largely unanswered. This aspect is now beginning to be understood in insect models, particularly in Drosophila melanogaster, with studies highlighting the importance of nutrient-responsive growth signaling pathways involving insulin/insulin-like growth factor signaling (IIS) and target of rapamycin (TOR) (IIS/TOR). These pathways operate in animals, from insects to mammals, adjusting the growth rate in response to the nutritional condition of the organism. Organismal growth is closely coupled with the process of developmental maturation mediated by maturation steroid hormones, which is influenced greatly by environmental and nutritional conditions. Recent Drosophila studies have been revealing the mechanisms responsible for this phenomenon. In this review, I summarize some important findings about the steroid hormone regulation of Drosophila body growth, calling attention to the influence of developmental nutritional conditions on animal size determination.     

Field estimates of fitness costs of the pace‐of‐life in an endangered damselfly

Theory predicts that within‐population differences in the pace‐of‐life can lead to cohort splitting and produce marked intraspecific variation in body size. Although many studies showed that body size is positively correlated with fitness, many argue that selection for the larger body is counterbalanced by opposing physiological and ecological selective mechanisms that favour smaller body. When a population split into cohorts with different paces of life (slow or fast cohort), one would expect to detect the fitness–size relationship among and within cohorts, that is, (a) slower‐developing cohort has larger body size and higher fitness than faster‐developing cohort, and (b) larger individuals within each cohort show higher fitness than smaller individuals. Here, we test these hypotheses in capture–mark–recapture field surveys that assess body size, lifespan, survival and lifetime mating success in two consecutive generations of a partially bivoltine aquatic insect, Coenagrion mercuriale, where the spring cohort is slower‐developing than the autumn cohort. As expected, body size was larger in the slow‐developing cohort, which is consistent with the temperature‐size rule and also with the duration of development. Body size seasonal variation was greater in slow‐developing cohort most likely because of the higher variation in age at maturity. Concordant with theory, survival probability, lifespan and lifetime mating success were higher in the slow‐developing cohort. Moreover, individual body size was positively correlated with survival and mating success in both cohorts. Our study confirms the fitness costs of fast pace‐of‐life and the benefits of larger body size to adult fitness.     

The evolution of large‐scale body size clines in Plethodon salamanders: evidence of heat‐balance or species‐specific artifact?

A major goal in macroecology is to determine how body size varies geographically, and explain why such patterns exist. Recently, a grid‐cell assemblage analysis found significant body size trends with latitude and temperature in Plethodon salamanders, and support for the heat‐balance hypothesis as a possible explanation for these trends. Here we demonstrate that the heat‐balance hypothesis is unlikely to have generated this pattern, and that there is no overall body size trend with temperature in Plethodon. Using data from 3155 local Plethodon assemblages, we find no support for body size clines with latitude, and no relationship between body size and temperature. We also found that body size did not covary with elevation, in contrast to what was predicted by heat‐balance. We then examined the various scenarios under which body size clines across grid‐cell assemblages could evolve via heat‐balance, and found that none were tenable in light of the existing data. Instead, a single, widely distributed species was responsible for the pattern across grid‐cell assemblages. Finally, we examined why phylogenetic eigenvector regression does not account for phylogenetic non‐independence among taxa, and should not be used to account for shared evolutionary history in assembly‐level analyses. Assemblage‐level patterns are a useful means of assessing biogeographic trends, and are an important complement to within‐species and cross‐species patterns. However, while the use of grid‐cell assemblage approaches from digital databases is expedient, their results must be examined critically, and whenever possible, compared with data obtained from local species assemblages (particularly for ecological mechanisms that operate at the level of individuals). Finally, our results emphasize the importance of using corroborative data to evaluate alternative hypotheses, so that potential mechanisms that explain bioegeographic patterns are properly assigned.     

Nutrition as a facilitator of host‐race formation: the shift of a stem‐boring beetle to a gall host

1. The importance of host‐race formation to herbivorous insect diversity depends on the likelihood that successful populations can be established on a new plant host. A previously unexplored ecological aid to success on a novel host is better nutritional quality. The role of nutrition was examined in the shift of the stem‐boring beetle Mordellistena convicta to fly‐induced galls on goldenrod and the establishment there of a genetically distinct gall host race. 2. First, larvae of the host race inhabiting stems of Solidago gigantea were transplanted into stems and galls of greenhouse‐grown S. gigantea plants. At the end of larval development, the mean mass of larvae transplanted to galls was significantly greater than the mass of larvae transplanted to stems, indicating a likely nutritional benefit during the shift. This advantage was slightly but significantly diminished when the gall‐inducing fly feeding at the centre of the gall died early in the season. Additionally, there was a suggestion of a trade‐off in the increased mortality of smaller beetle larvae transplanted into galls. 3. In a companion experiment, S. gigantea gall‐race beetle larvae were likewise transplanted to S. gigantea stems and galls. Besides the expected greater mass in galls, the larvae also exhibited adaptations to the gall nutritional environment: larger inherent size, altered tunnelling behaviour, and no diminution of mass pursuant to gall‐inducer mortality. 4. In a third line of inquiry, chemical analyses of field‐collected S. gigantea plants revealed higher levels of mineral elements important to insect nutrition in galls as compared with stems.     

Genome‐wide characterization and developmental expression profiling of long non‐coding RNAs in Sogatella furcifera

The genome‐wide characterization of long non‐coding RNA (lncRNA) in insects demonstrates their importance in fundamental biological processes. Essentially, an in‐depth understanding of the functional repertoire of lncRNA in insects is pivotal to insect resources utilization and sustainable pest control. Using a custom bioinformatics pipeline, we identified 1861 lncRNAs encoded by 1852 loci in the Sogatella furcifera genome. We profiled lncRNA expression in different developmental stages and observed that the expression of lncRNAs is more highly temporally restricted compared to protein‐coding genes. More up‐regulated Sogatella furcifera lncRNA expressed in the embryo, 4th and 5th instars, suggesting that increased lncRNA levels may play a role in these developmental stages. We compared the relationship between the expression of Sogatella furcifera lncRNA and its nearest protein gene and found that lncRNAs were more correlated to their downstream coding neighbors on the opposite strand. Our genome‐wide profiling of lncRNAs in Sogatella furcifera identifies exciting candidates for characterization of lncRNAs, and also provides information on lncRNA regulation during insect development.     

Carbon dioxide‐ and temperature‐mediated changes in plant defensive compounds alter food utilization of herbivores

Although the impact of elevated carbon dioxide and rising temperature on plants and animals has been extensively documented recently, only limited understanding exists regarding their combined effects. The objective of this research was to address the consequences of using combinations of elevated CO₂ and elevated temperature on a plant's defensive chemistry, and subsequent utilization of the plant as insect food. Our results indicated that elevated CO₂ and increased temperature, for the most part, act independently on the production of defensive compounds in broccoli leaves (Brassica oleracea L. var. italica). CO₂ concentrations had significant effects on the foliar water content, total phenolic compounds, polyphenol oxidase and trypsin inhibitor concentrations. The herbivore Spodoptera litura (Fabricius; Lepidoptera: Noctuidae) responded to changes in the plant secondary chemistry, with larvae consuming more plant materials that had been exposed to elevated CO₂. The food utilization efficiencies of second‐instar larvae were more sensitive to CO₂‐treated foliage than those of the third‐ and fourth‐instar larvae. Temperature did exert a significant effect on food utilization (ECD) by the larvae. Our study will provide important information in future predictions on plant–insect interactions as a result of climate change. The study also demonstrated that since various larval stages might respond differently to climate change, this possibility needs to be considered in future forecasting and monitoring.     

Catch‐up growth in the rhinoceros beetle Trypoxylus dichotomus (Coleoptera: Scarabaeidae): Smaller neonates gain relatively more body mass during larval development

Body size often varies among conspecific neonates. As larger adults generally have higher fitness than smaller conspecifics, it is adaptive for smaller neonates to subsequently gain relatively more size increments during larval development (catch‐up growth). Although catch‐up growth has been suggested in insects, inappropriate methods have been used to examine the size dependence of growth increments. Therefore, it remains unclear to what extent catch‐up growth is common among insects. The present study examined the size dependence of growth increments among larvae of Trypoxylus dichotomus using reduced major axis regression of final to initial body masses. Catch‐up growth was found consistently for larval instars. Furthermore, simulations of the size increments revealed that not only sexual divergence of the mean size, but also catch‐up growth within sexes plays a role in the development of sexual divergence in the body size distribution of T. dichotomus. The significance of catch‐up growth in body size evolution was discussed.     

The temperature‐size rule in Daphnia magna across different genetic lines and ontogenetic stages: Multiple patterns and mechanisms

Ectotherms tend to grow faster, but reach a smaller size when reared under warmer conditions. This temperature‐size rule (TSR) is a widespread phenomenon. Despite the generality of this pattern, no general explanation has been found. We therefore tested the relative importance of two proposed mechanisms for the TSR: (1) a stronger increase in development rate relative to growth rate at higher temperatures, which would cause a smaller size at maturity, and (2) resource limitation placing stronger constraints on growth in large individuals at higher temperatures, which would cause problems with attaining a large size in warm conditions. We raised Daphnia magna at eight temperatures to assess their size at maturity, asymptotic size, and size of their offspring. We used three clonal lines that differed in asymptotic size and growth rate. A resource allocation model was developed and fitted to our empirical data to explore the effect of both mechanisms for the TSR. The genetic lines of D. magna showed different temperature dependence of growth and development rates resulting in different responses for size at maturity. Also, at warm temperatures, growth was constrained in large, but not in small individuals. The resource allocation model could fit these empirical data well. Based on our empirical results and model explorations, the TSR of D. magna at maturity is best explained by a stronger increase in development rate relative to growth rate at high temperature, and the TSR at asymptotic size is best explained by a size‐dependent and temperature‐dependent constraint on growth, although resource limitation could also affect size at maturity. In conclusion, the TSR can take different forms for offspring size, size at maturity, and asymptotic size and each form can arise from its own mechanism, which could be an essential step toward finding a solution to this century‐old puzzle.