Shift in life-history strategy from reproduction to defense with colony age in the galling aphidHemipodaphis persimilis producing defensive first-instar larvae

Colony defense in some aphids is performed by sterile soldiers but in others by monomorphic larvae of a specific instar stage. This paper, focusing on a galling aphid Hemipodaphis persimilis with monomorphic defensive first instars, examined the mechanism by which the proportion of defenders is regulated in the colonies. Demographic analyses showed that the ratios of first instars (defenders) were kept constantly high (58% on average) from mid June to late September. High proportions of first instars could be explained by consistently high birth rates (birth rate hypothesis) or by a prolonged duration of the first instar stage (instar span hypothesis). With the progress of colony age, the mature-embryo content of apterous adults, used as an index of the birth rate, decreased and the proportions of advanced instars increased. These results did not support the birth rate hypothesis. By contrast, calculation of a newly proposed index, the molting rate, showed that the duration of the first-instar stage was short in incipient galls but became longer with colony age. The duration of other instar stages was always kept short. These results corroborate the instar span hypothesis and suggest that the prolongation of the first-instar stage is an adaptive mechanism by which the defender ratio is kept high in mature colonies where the birth rate is declining. The frequency of aggressive behavior in first instars increased from incipient to mature galls. Seasonal changes in the instar span and aggressiveness of first instars suggest that in H. persimilis colonies there is a strategic shift from the reproductive to defensive phase with colony age.     

Maternal death relaxes developmental inhibition in nymphal aphid defenders

In certain aphids, first-instar nymphs defend their gall by attacking intruding arthropod predators. One correlate of such defensive behaviour is a lengthened duration of the first nymphal stadium during the galling phase of the life cycle. A prolonged first stadium allows a large army of first-instar defenders to accumulate, which may be advantageous for gall defence. The factors determining developmental delay have been unclear, however. Our field experiment with Pemphigus obesinymphae, a North American gall-forming aphid with defensive first-instar nymphs, tests whether first-stadium duration is influenced by the death of the colony''s fundatrix (mother). We killed fundatrices in certain galls, left those in control galls alive, and counted aphids in each stadium in each gall. Galls in which fundatrices were killed contained a lower proportion of first-instar defenders and more late-instar nymphs than did galls with living fundatrices, indicating that maternal death dramatically increased developmental rate of nymphs. Possibly nymphal aphids respond adaptively to environmental cues that signal a threat to the colony''s welfare. Alternatively, the fundatrix actively suppresses offspring development in order to maintain a large army of soldiers to protect her gall. The results add a new layer of complexity to our understanding of social aphid systems.     

The use of kairomones for foraging decisions by an aphid parasitoid in small host aggregations

1. The wasp Diaeretiella rapae uses honeydew emitted by its host, the cabbage aphid Brevicoryne brassica, as a kairomone (chemicals emitted by an organism as part of its activity and used by its natural enemies to their advantage). The role of the kairomone in foraging decisions by the parasitic wasp was explored by manipulating the amount of honeydew and the number of aphids in a colony independently. The count-down patch-exploitation mechanism (Iwasa et al., 1981) was employed to predict the results of these manipulations and contrast them with the predictions of Waage's (1979) model. 2. Kairomonal activity of honeydew decreased as the honeydew aged and lost its activity completely within 72 h. 3. The wasp was exposed to different amounts of honeydew on (a) aphid-free leaves and (b) leaves bearing colonies of 150 aphids. The parasitoid search time on both leaf types increased with increasing honeydew contamination. On aphid-bearing leaves, the number of attacked aphids in the colonies also increased with increasing honeydew contamination. The presence of aphids reduced the parasitoid search time compared to search time on aphid-bearing leaves with the same level of honeydew contamination, as predicted by the count-down model. 4. Parasitoids exposed to the same amount of honeydew, but a different number of aphids in a colony on the leaf, first increased the number of aphids attacked in relation to the number of aphids in the colony. But as the colony reached a certain size, the number of aphids attacked levelled off, despite the increase in the number of aphids in the colony. Search time was variable but did not exhibit any trend as the number of aphids in the colonies increased. 5. These results suggest that honeydew level is used by D. rapae as a cue for assessment of the number of aphids in the colony. In such cases, a count-down exploitation mechanism gives the best results to a forager. Many parasitoids may use kairomones for patch assessment and will therefore employ a count-down rule during patch exploitation.     

FEMALE-BIASED SEX RATIOS IN A FACULTATIVELY SOCIAL BEE AND THEIR IMPLICATIONS FOR SOCIAL EVOLUTION

Montane populations of the Australian allodapine bee, Exoneura bicolor, are characterized by high levels of cooperative nesting and strongly female-biased sex ratios. A conspecific population from heathland shows much lower levels of cooperative nesting and lower levels of female bias. In both habitats, sex-ratio bias is greatest in the smallest brood sizes and becomes successively less biased in larger broods. Parity is approached in the largest heathland colonies, but not for any brood-size category in montane areas. Adult intracolony relatedness is moderately high for colonies in both reused and newly founded nests in the montane habitat, but probably low or zero for newly founded nests in heathland. Colony efficiency, measured as the number of brood per adult, increases with colony size in both habitats, suggesting that cooperation between females increases mean female fitness. It is argued that patterns of sex allocation are consistent with nonlinear fitness-return models, in which the mean reproductive value of daughters increases with the number of daughters produced in a brood. Such increases probably arise from a number of social interactions, including cooperative brood defense, increased task efficiency, and lower per capita costs in nest construction. The term “local fitness enhancement” is introduced here to describe these effects collectively. The female-biased ratios should lower selective thresholds for sib-directed altruism, at least in the earlier stages of colony development. It is argued that local fitness enhancement facilitates eusociality in allodapine bees and could also play a role in other haplodiploid taxa, provided cooperative nesting largely involves sisters, colony efficiency increases with colony size, and optimal colony sizes are only achieved after two or more generations after founding.     

An alternative pathway to eusociality: Exploring the molecular and functional basis of fortress defense

Some animals express a form of eusociality known as “fortress defense,” in which defense rather than brood care is the primary social act. Aphids are small plant‐feeding insects, but like termites, some species express division of labor and castes of aggressive juvenile “soldiers.” What is the functional basis of fortress defense eusociality in aphids? Previous work showed that the acquisition of venoms might be a key innovation in aphid social evolution. We show that the lethality of aphid soldiers derives in part from the induction of exaggerated immune responses in insects they attack. Comparisons between closely related social and nonsocial species identified a number of secreted effector molecules that are candidates for immune modulation, including a convergently recruited protease described in unrelated aphid species with venom‐like functions. These results suggest that aphids are capable of antagonizing conserved features of the insect immune response, and provide new insights into the mechanisms underlying the evolution of fortress defense eusociality in aphids.     

Social structure and the defensive role of soldiers in a eusocial bamboo aphid,Pseudoregma bambucicola (Homoptera: Aphididae): A test of the defence-optimization hypothesis

A complete understanding of the evolution of sociality in aphids requires a detailed knowledge of the patterns of soldier investment in their ecology. The eusocial bamboo aphidPseudoregma bambucicola has a morphologically specialized first-instar soldier caste. The proportion of soldiers was positively correlated with colony size. Within a colony, soldiers were evenly distributed among subcolonies; within each subcolony, however, their distribution was biased toward peripheries which were exposed to many predators. Field experiments introducing natural enemies such asEupeodes confrater (Diptera: Syrphidae) andSynonycha grandis (Coleoptera: Coccinellidae) revealed that the survival rate of these predators was negatively correlated with the density of soldiers, suggesting that soldiers can more or less defend their colonies by killing or removing a range of natural enemies. Observations suggest that large mature colonies attract more predators than newly established small colonies and that, within a colony, the predators attack each subcolony regardless of its position on bamboo shoots. This implies the presence of a positive correlation between colony size and predation risk. Thus, the investment in soldiers seems to reflect the attacking pattern of predators within a colony. These results agree with the defence-optimization hypothesis in soldier investment ofP. bambucicola colonies.     

Evaluation of counting error due to colony masking in bioaerosol sampling.

Colony counting error due to indistinguishable colony overlap (i.e., masking) was evaluated theoretically and experimentally. A theoretical model to predict colony masking was used to determine colony counting efficiency by Monte Carlo computer simulation of microorganism collection and development into CFU. The computer simulation was verified experimentally by collecting aerosolized Bacillus subtilis spores and examining micro- and macroscopic colonies. Colony counting efficiency decreased (i) with increasing density of collected culturable microorganisms, (ii) with increasing colony size, and (iii) with decreasing ability of an observation system to distinguish adjacent colonies as separate units. Counting efficiency for 2-mm colonies, at optimal resolution, decreased from 98 to 85% when colony density increased from 1 to 10 microorganisms cm-2, in contrast to an efficiency decrease from 90 to 45% for 5-mm colonies. No statistically significant difference (alpha = 0.05) between experimental and theoretical results was found when colony shape was used to estimate the number of individual colonies in a CFU. Experimental colony counts were 1.2 times simulation estimates when colony shape was not considered, because of nonuniformity of actual colony size and the better discrimination ability of the human eye relative to the model. Colony surface densities associated with high counting accuracy were compared with recommended upper plate count limits and found to depend on colony size and an observation system's ability to identify overlapped colonies. Correction factors were developed to estimate the actual number of collected microorganisms from observed colony counts.(ABSTRACT TRUNCATED AT 250 WORDS)     

Defense of Food Supply by Eusocial Colonies

Overdispersion of colonies exists in many eusocial insects.Overdispersion can be generated by direct attack on coloniesor founders, by defense of space, by defense of food resourcesbeing harvested, or by exploitative competition. When directcompetitive interactions lead to colony overdispersion, territorialityis said to occur. Whereas solitary territory holders typicallydefend space, most eusocial colonies defend resource patchesrather than space per se. Also unlike solitary territory holders,colonies with forager communication can simultaneously defendseveral spatially separated food patches. A model explores optimalnumbers of scouts (discoverers of patches) and recruits (followers)needed to maximize net rate of energy intake by the colony.Territorial costs are added to the model by requiring a higherinvestment of foragers per unit resource collected. Accordingto the model, optimal colony size and percentage scouts aremore sensitive to changes in patch size than in patch density.If patch defense is required for resource control, a declineoccurs in optimal percentage of scouts; the decline is greatestfor small colonies. Colonies that must defend patches in orderto harvest from them suffer a loss in net energy intake; theloss is greatest for small colonies. It is predicted that amongeusocial insects, those with territorial defense of resourcesshould preferentially visit large patches and have comparativelylarge colony sizes and relatively few scouts. Ways of testingthese predictions are discussed.     

Clonal mixing in the soldier-producing aphid Pemphigus spyrothecae (Hemiptera: Aphididae)

Illuminating the genetic relationships within soldier-producing aphid colonies is an essential element of any attempt to explain the evolution of the altruistic soldier caste. Pemphigus spyrothecae is a soldier-producing aphid that induces galls on the leaf petioles of its host (trees of the genus Populus). At least a quarter of the aphids within the clonally produced gall population are morphologically and behaviourally distinct first-instar soldiers that defend the gall population from predation. Using field trapping and microsatellites, we investigated the degree of clonal mixing within natural gall populations. Field trapping in the UK showed that all the migrants of P. spyrothecae and of two other Pemphigus species were wingless first-instar soldiers. The average degree of mixing estimated from trapping P. spyrothecae migrants was 0.68% (range = 0-15%). Microsatellite genotyping of 277 aphids from 13 galls collected in Italy revealed an average mixing level of 10.4% (range = 0-59%). Six galls contained more than one clone (range = 2-5 clones). Non-kin aphids were not restricted to the soldier caste but were evenly distributed across instars. An additional gall, from which 527 occupants were genotyped, contained 12 non-kin aphids distributed among nine clones, showing that clonal diversity can be high even when mixing is very low. These observations suggest that although soldiers migrate regularly and can moult and reproduce within foreign galls, clonal mixing in this species is generally low and is unlikely to provide a barrier to the evolution of investment by the aphid clones in an altruistic soldier caste.     

Geographic variation of caste structure among ant populations

Morphologically distinct worker castes of eusocial insects specialize in different tasks. The relative proportions of these castes and their body sizes represent the demography of a colony that is predicted to vary adaptively with environments. Despite strong theoretical foundations, there has been little empirical evidence for the evolution of colony demography in nature. We show that geographically distinct populations of the ant Pheidole morrisi differ in worker caste ratios and worker body sizes in a manner consistent with microevolutionary divergence. We further show that the developmental mechanism for caste determination accounts for the unique pattern of covariation observed in these two traits. Behavioral data reveal that the frequency of different tasks performed by workers changes in a caste-specific manner when caste ratios are altered and demonstrate the importance of the major caste in colony defense. The population-level variation documented here for P. morrisi colonies supports the predictions of adaptive demography theory and illustrates that developmental mechanisms can play a significant role in shaping the evolution of phenotype at the colony level.     

Buying time for colony mates: the anti-predatory function of soldiers in the eusocial aphid Ceratovacuna japonica (Homoptera, Hormaphidinae)

Eusocial aphids produce sterile individuals (soldiers) that specialize in colony protection. Killing predators is often considered the main function of soldiers. In this study, we tested the effect of harassment by soldiers of a eusocial aphid, Ceratovacuna japonica (Homoptera, Hormaphidinae), on predation by this species’ natural enemy, the larvae of Atkinsonia ignipicta (Lepidoptera, Stathmopodidae). We experimentally introduced some aphids and a predator to petri dishes and compared the survivorship of first-instar reproductives in the presence and absence of soldiers. We showed that soldiers can reduce the rate of predation on their colony mates without killing the predators. When predators encountered soldiers, they did not attempt to prey on them. Instead, they evaded them and often started to make a nest by spinning silken threads. The soldiers, in contrast, waved their forelegs and attacked the predator, and they sometimes succeeded in grasping the predator’s body. Because the predator used its mandibles to remove any soldier that succeeded in grasping its body, the soldier did not kill the predator. The reduction of predation was apparently caused by the delay of predation resulting from the harassment behavior of the soldiers. In eusocial aphids, a defensive strategy that delays predation may buy the soldiers’ colony mates time to reproduce or to escape from the predator.     

The effects of colony characteristics on life span and foraging behavior of individual wasps (Polybia occidentalis,Hymenoptera: Vespidae)

Summary We studied the effects of intrinsic colony characteristics and an imposed contingency on the life span and behavior of foragers in the swarm-founding social waspPolybia occidentalis. Data were collected on marked, known-age workers introduced into four observation colonies.To test the hypothesis that colony demographic features affect worker life span, we examined the relationships of colony age and size with worker life span using survivorship analysis. Colony age and size had positive relationships with life span; marked workers from two larger, older colonies had longer life spans (¯X = 24.7 days) than those from two smaller, younger colonies (¯X = 20.1 days).We quantified the effects of experimentally imposed nest damage on forager behavior, to determine which of three predicted behavioral responses by foragers to this contingency (increased probability of foraging for building material, increased rate of foraging, or decrease in age of onset of foraging) would be employed. Increasing the colony level of need for materials used in nest construction (wood pulp and water) by damaging the nests of two colonies did not cause an increase in either the proportion of marked workers that gathered nest materials or in foraging rates of marked individuals, when compared with introduced workers in two simultaneously observed control colonies. Instead, nest damage caused a decrease in the age at which marked workers first foraged for pulp and water. The response to an increase in the need for building materials was an acceleration of behavioral development in some workers.     

Caste allometries in the soldier-producing aphidPseudoregma alexanderi (Hormaphididae: Aphidoidea)

Summary Colonies of the aphidPseudoregma alexanderi produce morphologically-specialized first-instar larvae, termed soldiers, that defend the colony from predators. The environmental cues and physiological mechanisms governing soldier production are currently unknown. Here we present a morphometric study of soldiers and normal first-instar larvae ofP. alexanderi. Several morphological features (fore-leg length and width, hind-leg length, and horn length) plotted against body length display relationship that are similar to a sigmoidal curve. We found further support for an earlier finding that soldiers fall into two size categories, majors and minors, although both types of soldiers appear to follow the same allometry. The patterns of allometry in the soldier-producing aphids are very different from those found in other social insects and do not easily fit into the traditional categorization of allometries. We present two simple alternative models of soldier development as a framework for guiding future studies of the mechanisms of soldier production.     

A review on self-destructive defense behaviors in social insects

Colony defense is a necessary but dangerous task for social insects, and nest defensive behaviors often lead to a premature death of the actor. As an extreme form of colony defense, self-sacrificial behaviors have evolved by kin selection in various social insects. Most self-sacrificial defensive mechanisms occur in response to an acute threat to the colony, but some behaviors are preemptive actions that avert harm to the colony. Self-sacrifice has also been observed as a form of preemptive defense against parasites and pathogens where individuals will abandon their normal colony function and die in self-exile to reduce the risk of infecting nestmates. Here, we provide an overview of the self-destructive defense mechanisms that eusocial insects have evolved and discuss avenues for future research into this form of altruism.     

Juvenile hormone as a regulator of the trade-off between reproduction and life span in Drosophila melanogaster

Trade-offs between reproduction and life span are ubiquitous, but little is known about their underlying mechanisms. Here we combine treatment with the juvenile hormone analog (JHa) methoprene and experimental evolution in Drosophila melanogaster to study the potential role of juvenile hormone (JH) in mediating such trade-offs at both the physiological and evolutionary level. Exposure to JHa in the larval medium (and up to 24 h posteclosion) increased early life fecundity but reduced life span of normal (unselected) flies, supporting the physiological role of JH in mediating the trade-off. This effect was much smaller for life span, and not detectable for fecundity, in fly lines previously bred for 19 generations on a medium containing JHa. Furthermore, these selection lines lived longer than unselected controls even in the absence of JHa treatment, without a detectable reduction in early life fecundity. Thus, selection for resistance to JHa apparently induced some evolutionary changes in JH metabolism or signaling, which led to longer life span as a correlated response. This supports the hypothesis that JH may mediate evolution of longer life span, but--contrary to our expectation-this apparently does not need to trade--off with fecundity.     

The relationship between conidial dose,moulting and insect developmental stage on the susceptibility of cotton aphid,Aphis gossypii,to conidia of Lecanicillium attenuatum,an entomopathogenic fungus

The cotton aphid is one of the most serious pests of greenhouse vegetable crops worldwide. It is difficult to control because field populations usually include simultaneously several insect developmental stages. The current research evaluated an isolate (CS625) of Lecanicillium attenuatum, a fungal pathogen of aphids, as to its virulence against different developmental stages of cotton aphid, Aphis gossypii. The influence on mortality of several other factors also was examined: (a) insect moulting, (b) the number of conidia attached to insect cuticles and (c) germination rates of conidia on cuticles of aphids at various developmental stages. Mortality of cotton aphids treated with L. attenuatum conidia varied according to the developmental stage of the host, i.e. the LT_50s with third-instar nymphs and adults was shorter than with first-instar nymphs. The number of spores attached to the surface of first-instar nymphs was approximately one-half of that on third-instar nymphs and adults. Also, the level of spore germination on the surface of first-instar nymphs was lower than on the surface of other stages of the aphid. After moulting, the numbers of conidia attached to new insect cuticles were less than on exuviae. These results suggest that early nymphal stages of cotton aphids may escape fungal disease due, at least in part, to a combination of three factors: low numbers of conidia attached to their cuticles; low levels of conidial germination and rapid ecdyses, which removed conidia before their germ tubes penetrated the host hemolymph.     

Life Span Evolution in Eusocial Workers—A Theoretical Approach to Understanding the Effects of Extrinsic Mortality in a Hierarchical System

While the extraordinary life span of queens and division of labor in eusocial societies have been well studied, it is less clear which selective forces act on the short life span of workers. The disparity of life span between the queen and the workers is linked to a basic issue in sociobiology: How are the resources in a colony allocated between colony maintenance and reproduction? Resources for somatic maintenance of the colony can either be invested into quality or quantity of workers. Here, we present a theoretical optimization model that uses a hierarchical trade-off within insect colonies and extrinsic mortality to explain how different aging phenotypes could have evolved to keep resources secure in the colony. The model points to the significance of two factors. First, any investment that would generate a longer intrinsic life span for workers is lost if the individual dies from external causes while foraging. As a consequence, risky environments favor the evolution of workers with a shorter life span. Second, shorter-lived workers require less investment than long-lived ones, allowing the colony to allocate these resources to sexual reproduction or colony growth.     

Domestication-related changes in sexual performance of Queensland fruit fly

In Sterile Insect Technique (SIT) programs, massive numbers of insects are reared, sterilized, and released in the field to impede reproduction of pest populations. The domestication and rearing processes used to produce insects for SIT programs may have significant evolutionary impacts on life history and reproductive biology. We assessed the effects of domestication on sexual performance of laboratory reared Queensland fruit fly, Bactrocera tryoni, by comparing an old (49 generations) and a young colony (5 generations). We evaluated mating propensity, mating latency, copula duration, sperm transfer, and ability to induce sexual inhibition in mates. Overall, both males and females from the old colony had greater mating propensity than those from the young colony. Copula duration was longer when females were from the old colony. There was no evidence of sexual isolation between the colonies as males and females from the two colonies had similar propensity to mate with flies from either colony. Males from the old colony transferred more sperm regardless of which colony their mate was from. Finally, males from both colonies were similarly able to induce sexual inhibition in their mates and were also similarly able to secure copulations with already-mated females. Positive effects of domestication on sperm transfer, coupled with maintained ability to induce sexual inhibition in mates and to secure copulations with previously mated females, highlights that domestication may have little effect, or even positive effects, on some aspects of sexual performance that may advantage mass-reared B. tryoni in SIT programs.     

Detection of the genetic effects of contraception

The sudden appearance of effective contraception in certain populations in the last decade has provided data useful for studying the genetic effect of contraception on our own generation and on future generations of the human race. Since 1948, Japan has halved its birthrate by therapeutic abortion, reducing the mean maternal age. Since 1965, Chile's contraception program has reduced the birthrate from 35 to 25 per 1000, increased the proportion of primiparas from 25% to 35%, increased the frequency of mothers aged less than 20 years from 13% to 20%, decreased the mean maternal age from 27.6 to 25.6 years and increased its variance, reduced infant mortality from 100 to 80 per 1000 live births, and reduced the number of stillbirths from 2.5% to 1.9%. Two changes predicted by genetic theory, decreases in mongolism and anencephaly, did not occur. Long-term genetic effects are poorly understood, except for studies on Japanese populations exposed to ionizing radiation. The only eugenic strategy we can apply for future generations is to conserve variation in the human genotype.     

Prey Abundance, Intraguild Predators, Ants and the Optimal Egg-laying Strategy of a Furtive Predator

Larval performance can have a great influence on female oviposition choice, especially in insects where the newly hatched offspring are unable to move any great distance to find an appropriate food source. For furtive predators, like the predatory midge Aphidoletes aphidimyza which preys on aphids while simultaneously residing and remaining undetected within their colonies, oviposition behaviour is crucial because these slow moving offspring are restrained to their natal colony. Here we develop a new model for predicting the optimum number of eggs that a furtive predator should lay in an aphid colony, based on: (1) the number of available prey (aphids); (2) the protection from predation conferred by “hiding” in the colony and (3) the effects of interspecific and intraspecific competition. We also explore the effect of aphid attendance by ants on oviposition behavior. We compare model predictions with empirical field observations of the clutch sizes of A. aphidimyza in apple orchards. The simplest of the four models best fits the observed data and provides the first field evidence that a furtive predator adjusts its clutch size as a function of prey density. The slope of the relationship between clutch size and aphid number is quite close to that predicted by our models suggesting that intra-clutch competition is the main factor governing furtive aphid midge oviposition choice.