Alate susceptibility in ants

Pathogens are predicted to pose a particular threat to eusocial insects because infections can spread rapidly in colonies with high densities of closely related individuals. In ants, there are two major castes: workers and reproductives. Sterile workers receive no direct benefit from investing in immunity, but can gain indirect fitness benefits if their immunity aids the survival of their fertile siblings. Virgin reproductives (alates), on the other hand, may be able to increase their investment in reproduction, rather than in immunity, because of the protection they receive from workers. Thus, we expect colonies to have highly immune workers, but relatively more susceptible alates. We examined the survival of workers, gynes, and males of nine ant species collected in Peru and Canada when exposed to the entomopathogenic fungus Beauveria bassiana. For the seven species in which treatment with B. bassiana increased ant mortality relative to controls, we found workers were significantly less susceptible compared with both alate sexes. Female and male alates did not differ significantly in their immunocompetence. Our results suggest that, as with other nonreproductive tasks in ant colonies like foraging and nest maintenance, workers have primary responsibility for colony immunity, allowing alates to specialize on reproduction. We highlight the importance of colony‐level selection on individual immunity in ants and other eusocial organisms.     

Larval food limitation in butterflies: effects on adult resource allocation and fitness

Allocation of larval food resources affects adult morphology and fitness in holometabolous insects. Here we explore the effects on adult morphology and female fitness of larval semi-starvation in the butterfly Speyeria mormonia. Using a split-brood design, food intake was reduced by approximately half during the last half of the last larval instar. Body mass and forewing length of resulting adults were smaller than those of control animals. Feeding treatment significantly altered the allometric relationship between mass and wing length for females but not males, such that body mass increased more steeply with wing length in stressed insects as compared to control insects. This may result in changes in female flight performance and cost. With regard to adult life history traits, male feeding treatment or mating number had no effect on female fecundity or survival, in agreement with expectations for this species. Potential fecundity decreased with decreasing body mass and relative fat content, but there was no independent effect of larval feeding treatment. Realized fecundity decreased with decreasing adult survival, and was not affected by body mass or larval feeding treatment. Adult survival was lower in insects subjected to larval semi-starvation, with no effect of body mass. In contrast, previous laboratory studies on adult nectar restriction showed that adult survival was not affected by such stress, whereas fecundity was reduced in direct 11 proportion to the reduction of adult food. We thus see a direct impact of larval dietary restriction on survival, whereas fecundity is affected by adult dietary restriction, a pattern reminiscent of a survival/reproduction trade-off, but across a developmental boundary. The data, in combination with previous work, thus provide a picture of the intra-specific response of a suite of traits to ecological stress.     

Social life-history response to individual immune challenge of workers of Bombus terrestris L.: a possible new cooperative phenomenon

Parasites typically reduce host survival or fecundity. To minimize fitness loss, hosts can make temporal adjustments of their reproductive effort. To date such plastic shifts of life‐history traits in response to parasitism are only known from solitary organisms where infected individuals can react by themselves. In the case of social insects, where brood care and reproductive effort is shared between reproductive individuals (typically the queen) and workers, adjustments of the reproductive effort would depend on collective decision‐making. We tested for this possibility by experimentally activating the immune response of individual workers in colonies of the bumblebee, Bombus terrestris L. This induction resulted, in combination with environmental conditions, in a reduction of fitness of the social unity (i.e. colony success, measured by number and biomass of offspring) and a collective response towards earlier reproduction. As both phenomena are expressed at the level of the colony, the result suggests that key elements of the use of immune defence have been maintained through the evolutionary transition to sociality.     

Colony performance and immunocompetence of a social insect, Bombus terrestris, in poor and variable environments

1. Feeding and defence against parasites are among the major simultaneous requirements for survival and successful reproduction of any animal, including colonies of social insects. Harsh environments may therefore not only negatively affect overall success, but force animals to allocate resources in different ways, for example, to reduce immune defence under adverse conditions while maintaining growth rate.
2. This study examines how colony growth, reproduction and immune defence of the bumble bee, Bombus terrestris , varies with environmental condition. In particular, the manner in which limited or unpredictable food availability affects the number and size of workers and sexuals produced, the timing of reproduction, and the level of encapsulation of a novel antigen was tested. A new experimental paradigm was applied by splitting colonies into two halves while ensuring integrity by regular swaps of the residing queen.
3. The results show that limited food availability, as expected, led to fewer and smaller workers and sexuals. Unpredictable food availability, in contrast, was associated with higher numbers of workers and heavier sexuals. Also, reproductive success was highest under unpredictable conditions, due to an increased rate of collection of resources.
4. The timing of reproduction did not vary among treatments. Contrary to expectation, also immunocompetence did not vary among treatments.     

Ant Colonies Do Not Trade-Off Reproduction against Maintenance

The question on how individuals allocate resources into maintenance and reproduction is one of the central questions in life history theory. Yet, resource allocation into maintenance on the organismic level can only be measured indirectly. This is different in a social insect colony, a “superorganism” where workers represent the soma and the queen the germ line of the colony. Here, we investigate whether trade-offs exist between maintenance and reproduction on two levels of biological organization, queens and colonies, by following single-queen colonies of the ant Cardiocondyla obscurior throughout the entire lifespan of the queen. Our results show that maintenance and reproduction are positively correlated on the colony level, and we confirm results of an earlier study that found no trade-off on the individual (queen) level. We attribute this unexpected outcome to the existence of a positive feedback loop where investment into maintenance (workers) increases the rate of resource acquisition under laboratory conditions. Even though food was provided ad libitum, variation in productivity among the colonies suggests that resources can only be utilized and invested into additional maintenance and reproduction by the colony if enough workers are available. The resulting relationship between per-capita and colony productivity in our study fits well with other studies conducted in the field, where decreasing per-capita productivity and the leveling off of colony productivity have been linked to density dependent effects due to competition among colonies. This suggests that the absence of trade-offs in our laboratory study might also be prevalent under natural conditions, leading to a positive association of maintenance, (= growth) and reproduction. In this respect, insect colonies resemble indeterminate growing organisms.     

Experimental increase in fecundity causes upregulation of fecundity and body maintenance genes in the fat body of ant queens

In most organisms, fecundity and longevity are negatively associated and the molecular regulation of these two life-history traits is highly interconnected. In addition, nutrient intake often has opposing effects on lifespan and reproduction. In contrast to solitary insects, the main reproductive individual of social hymenopterans, the queen, is also the most long-lived. During development, queen larvae are well-nourished, but we are only beginning to understand the impact of nutrition on the queens'' adult life and the molecular regulation and connectivity of fecundity and longevity. Here, we used two experimental manipulations to alter queen fecundity in the ant Temnothorax rugatulus and investigated associated changes in fat body gene expression. Egg removal triggered a fecundity increase, leading to expression changes in genes with functions in fecundity such as oogenesis and body maintenance. Dietary restriction lowered the egg production of queens and altered the expression of genes linked to autophagy, Toll signalling, cellular homeostasis and immunity. Our study reveals that an experimental increase in fecundity causes the co-activation of reproduction and body maintenance mechanisms, shedding light on the molecular regulation of the link between longevity and fecundity in social insects.     

Trade‐offs in the evolution of bumblebee colony and body size: a comparative analysis

Trade‐offs between life‐history traits – such as fecundity and survival – have been demonstrated in several studies. In eusocial insects, the number of organisms and their body sizes can affect the fitness of the colony. Large‐than‐average body sizes as well as more individuals can improve a colony's thermoregulation, foraging efficiency, and fecundity. However, in bumblebees, large colonies and large body sizes depend largely on high temperatures and a large amount of food resources. Bumblebee taxa can be found in temperate and tropical regions of the world and differ markedly in their colony sizes and body sizes. Variation in colony size and body size may be explained by the costs and benefits associated with the evolutionary history of each species in a particular environment. In this study, we explored the effect of temperature and precipitation (the latter was used as an indirect indicator of food availability) on the colony and body size of twenty‐one bumblebee taxa. A comparative analysis controlling for phylogenetic effects as well as for the body size of queens, workers, and males in bumblebee taxa from temperate and tropical regions indicated that both temperature and precipitation affect colony and body size. We found a negative association between colony size and the rainiest trimester, and a positive association between the colony size and the warmest month of the year. In addition, male bumblebees tend to evolve larger body sizes in places where the rain occurs mostly in the summer and the overall temperature is warmer. Moreover, we found a negative relationship between colony size and body sizes of queens, workers, and males, suggesting potential trade‐offs in the evolution of bumblebee colony and body size.     

Are there interactive effects of mate availability and predation risk on life history and defence in a simultaneous hermaphrodite?

Encountering mates and avoiding predators are ubiquitous challenges faced by many organisms and they can affect the expression of many traits including growth, timing of maturity and resource allocation to reproduction. However, these two factors are commonly considered in isolation rather than simultaneously. We examined whether predation risk and mate availability interact to affect morphology and life-history traits (including lifetime fecundity) of a hermaphroditic snail (Physa acuta). We found that mate availability reduced juvenile growth rate and final size. Predator cues from crayfish induced delayed reproduction, but there were no reduced fecundity costs associated with predator induction. Although there were interactive effects on longevity, lifetime fecundity was determined by the number of reproductive days. Therefore, our results indicate a resource-allocation trade-off among growth, longevity and reproduction. Future consideration of this interaction will be important for understanding how resource-allocation plasticity affects the integration of defensive, life-history and mating-system traits.     

Yoyo-bang: a risk-aversion investment strategy by a perennial insect society

In 1978, Oster and Wilson proposed a bang-bang investment strategy for social insects in which colony size at maturity amplifies colony reproduction. In this paper, the investment strategies of the monogyne form of the fire ant, Solenopsis invicta, were compared to the predictions of the bang-bang model. Demographic census data, collected on fire ant mounds excavated every month during the years 1985 and 1988, revealed that colony reproduction was independent of colony size (~50,000 to ~250,000 workers). Why were mature S. invicta colonies up to five times larger than they needed to be to reproduce an annual batch of sexual offspring? To address this question, Oster and Wilson's bang-bang model was modified to a "yoyo-bang" investment strategy for perennial societies. In the yoyo-bang model, excess workers are a disposable reserve - a buffer - that can oscillate up or down depending on resource availability without adversely affecting annual reproductive cycles. The yoyo-bang model links colony size, colony survival and lifetime reproductive fitness.     

Bridging Developmental Boundaries: Lifelong Dietary Patterns Modulate Life Histories in a Parthenogenetic Insect

Determining the effects of lifelong intake patterns on performance is challenging for many species, primarily because of methodological constraints. Here, we used a parthenogenetic insect (Carausius morosus) to determine the effects of limited and unlimited food availability across multiple life-history stages. Using a parthenogen allowed us to quantify intake by juvenile and adult females and to evaluate the morphological, physiological, and life-history responses to intake, all without the confounding influences of pair-housing, mating, and male behavior. In our study, growth rate prior to reproductive maturity was positively correlated with both adult and reproductive lifespans but negatively correlated with total lifespan. Food limitation had opposing effects on lifespan depending on when it was imposed, as it protracted development in juveniles but hastened death in adults. Food limitation also constrained reproduction regardless of when food was limited, although decreased fecundity was especially pronounced in individuals that were food-limited as late juveniles and adults. Additional carry-over effects of juvenile food limitation included smaller adult size and decreased body condition at the adult molt, but these effects were largely mitigated in insects that were switched to ad libitum feeding as late juveniles. Our data provide little support for the existence of a trade-off between longevity and fecundity, perhaps because these functions were fueled by different nutrient pools. However, insects that experienced a switch to the limited diet at reproductive maturity seem to have fueled egg production by drawing down body stores, thus providing some evidence for a life-history trade-off. Our results provide important insights into the effects of food limitation and indicate that performance is modulated by intake both within and across life-history stages.     

Changes in maternal investment in eggs can affect population dynamics

The way that mothers provision their offspring can have important consequences for their offspring's performance throughout life. Models suggest that maternally induced variation in life histories may have large population dynamical effects, even perhaps driving cycles such as those seen in forest Lepidoptera. The evidence for large maternal influences on population dynamics is unconvincing, principally because of the difficulty of conducting experiments at both the individual and population level. In the soil mite, Sancassania berlesei, we show that there is a trade-off between a female's fecundity and the per-egg provisioning of protein. The mother's position on this trade-off depends on her current food availability and her age. Populations initiated with 250 eggs of different mean sizes showed significant differences in the population dynamics, converging only after three generations. Differences in the growth, maturation and fecundity of the initial cohort caused differences in the competitive environment for the next generation, which, in turn, created differences in their growth and reproduction. Maternal effects in one generation can therefore lead to population dynamical consequences over many generations. Where animals live in environments that are temporally variable, we conjecture that maternal effects could result in long-term dynamical effects.     

Immune responses of bumblebee workers as a function of individual and colony age: senescence versus plastic adjustment of the immune function

Senescence may evolve in response to externally imposed schedules of survival and reproduction. It may result from cumulative damage to several tissues and organs leading to the progressive malfunction of somatic defences including the immune system, which is a relevant and accessible trait to study the evolution and the mechanisms of senescence.
In social insects, reproduction of workers is negligible and their fitness relies on the colony reproductive success, which depends on workers' longevity. Consequently, evolution of senescence in workers will rely on age-dependent survival rate and the residual reproductive value of the colony. Using the bumblebee, Bombus terrestris , as model system, we investigated changes in constitutive and inducible immune defences. Such changes were monitored in relation to worker age and colony age and as well under a high, persistent level of parasitism. The results show that the inducible production of antibacterial peptides was not affected by the age of individual worker or the age of their colony. In contrast, constitutive defences such as haemocyte density and phenoloxidase (PO) activity decline with individual worker age and potential accumulation of physiological defects due to high and persistent levels of parasitism did not explain this pattern of immunosenescence. Interestingly, levels of worker constitutive defences were found to increase with colony age. We found antibacterial activity was strongly traded-off against PO activity. Such a relationship was not caused by resource shortage. Overall, these data suggest that patterns of variation of immune defences with worker age and colony age are likely the result of plastic temporal adjustments of immune responses in accordance with life history predictions. Hence, control of pathogenic threat in a social system may involve optimal adjustments of immune defences at both the individual and colony levels.     

Effects of resource availability and social parasite invasion on field colonies of Bombus terrestris

Abstract.  1. The survival, growth and fecundity of bumblebee colonies are affected by the availability of food resources and presence of natural enemies. Social parasites (cuckoo bumblebees and other bumblebees) can invade colonies and reduce or halt successful reproduction; however, little is known about the frequency of invasion or what environmental factors determine their success in the field.
2. We used 48 experimental colonies of the bumblebee Bombus terrestris , and manipulated both resource availability at the landscape scale and date of colony founding, to explore invasion rates of social parasites and their effect on the performance of host colonies.
3. Proximity to abundant forage resources (fields of flowering oilseed rape) and early colony founding significantly increased the probability of parasite invasion and thus offset the potential positive effects of these factors on bumblebee colony performance.
4. The study concludes that optimal colony location may be among intermediate levels of resources and supports schemes designed to increase the heterogeneity of forage resources for bumblebees across agricultural landscapes.     

Conflict over male parentage in social insects

Mutual policing is an important mechanism that maintains social harmony in group-living organisms by suppressing the selfish behavior of individuals. In social insects, workers police one another (worker-policing) by preventing individual workers from laying eggs that would otherwise develop into males. Within the framework of Hamilton's rule there are two explanations for worker-policing behavior. First, if worker reproduction is cost-free, worker-policing should occur only where workers are more closely related to queen- than to worker-produced male eggs (relatedness hypothesis). Second, if there are substantial costs to unchecked worker reproduction, worker-policing may occur to counteract these costs and increase colony efficiency (efficiency hypothesis). The first explanation predicts that patterns of the parentage of males (male parentage) are associated with relatedness, whereas the latter does not. We have investigated how male parentage varies with colony kin structure and colony size in 50 species of ants, bees, and wasps in a phylogenetically controlled comparative analysis. Our survey revealed that queens produced the majority of males in most of the species and that workers produced more than half of the males in less than 10% of species. Moreover, we show that male parentage does not vary with relatedness as predicted by the relatedness hypothesis. This indicates that intra- and interspecific variation in male parentage cannot be accounted for by the relatedness hypothesis alone and that increased colony efficiency is an important factor responsible for the evolution of worker-policing. Our study reveals greater harmony and more complex regulation of reproduction in social insect colonies than that expected from simple theoretical expectations based on relatedness only.     

Immediate and delayed life history effects caused by food deprivation early in life in a short‐lived lizard

Detailed studies of the mechanisms driving life history effects of food availability are of prime importance to understand the evolution of phenotypic plasticity and the capacity of organisms to produce better adapted phenotypes. Food availability may influence life history trajectories through three nonexclusive mechanisms: (i) immediate and long‐lasting effects on individual quality, and indirect delayed effects on (ii) intracohort and (iii) intercohort interactions. Using the common lizard (Zootoca vivipara), we tested whether a food deprivation during the two‐first months of life influence life history (growth, survival, reproduction) and performance traits (immunocompetence, locomotor performances) until adulthood. We investigated the underlying mechanisms and their possible interactions by manipulating jointly food availability in a birth cohort and in cohorts of older conspecifics. Food deprivation had direct immediate negative effects on growth but positive long‐lasting effects on immunocompetence. Food deprivation had also indirect delayed effects on growth, body size, early survival and reproduction mediated by an interaction between its direct effects on individual quality and its delayed effects on the intensity of intercohort social interactions combined with density dependence on body size. These results demonstrate that interactions between direct and socially mediated effects of past environments influence life history evolution in size‐structured and stage‐structured populations.     

Salt intake in Amazonian ants: too much of a good thing?

Although herbivory is widespread among insects, plant tissues rarely provide the optimal balance of nutrients for insect growth and reproduction. As a result, many herbivorous insects forage elsewhere for particular amino acids and minerals. Recent studies have shown that both herbivory and recruitment to sodium are commonplace among tropical rainforest ants, but little is known about how ants regulate their sodium intake at the individual and colony levels. In social insects, foragers may respond not only to their own nutritional deficiencies but also to those of their nestmates, who may have different nutritional requirements depending on their developmental stage, sex, or caste. Here, we investigate how salt stress among rainforest ants affects their preferences for salt and subsequent survival. We found that ants recruited more to salt than to any other bait type tested, confirming the strong preference for salt of ants in this region. Initially, we observed similarly high recruitment to salt among workers of the arboreal, herbivorous/omnivorous ant species Camponotus mirabilis. However, when provided with unrestricted access to high concentrations of salt, C. mirabilis workers suffered significantly higher mortality relative to controls, suggesting that C. mirabilis workers forage for sodium to the point of toxicity. Nonetheless, surviving workers showed reduced preference for salt at the end of the experiment, so some but not all individuals were able to regulate their salt intake beneath lethal dosages. We discuss how salt intake regulation may depend on colony members other than workers.     

Resource availability modulates the effect of body size on reproductive development

Within-species variation in animal body size predicts major differences in life history, for example, in reproductive development, fecundity, and even longevity. Purely from an energetic perspective, large size could entail larger energy reserves, fuelling different life functions, such as reproduction and survival (the “energy reserve” hypothesis). Conversely, larger body size could demand more energy for maintenance, and larger individuals might do worse in reproduction and survival under resource shortage (the “energy demand” hypothesis). Disentangling these alternative hypotheses is difficult because large size often correlates with better resource availability during growth, which could mask direct effects of body size on fitness traits. Here, we used experimental body size manipulation in the freshwater cnidarian Hydra oligactis, coupled with manipulation of resource (food) availability to separate direct effects of body size from resource availability on fitness traits (sexual development time, fecundity, and survival). We found significant interaction between body size and food availability in sexual development time in both males and females, such that large individuals responded less strongly to variation in resource availability. These results are consistent with an energy reserve effect of large size in Hydra. Surprisingly, the response was different in males and females: small and starved females delayed their reproduction, while small and starved males developed reproductive organs faster. In case of fecundity and survival, both size and food availability had significant effects, but we detected no interaction between them. Our observations suggest that in Hydra, small individuals are sensitive to fluctuations in resource availability, but these small individuals are able to adjust their reproductive development to maintain fitness.     

Fitness and the level of homozygosity in a social insect

To date very few studies have addressed the effects of inbreeding in social Hymenoptera, perhaps because the costs of inbreeding are generally considered marginal owing to male haploidy whereby recessive deleterious alleles are strongly exposed to selection in males. Here, we present one of the first studies on the effects of queen and worker homozygosity on colony performance. In a wild population of the ant Formica exsecta, the relative investment of single‐queen colonies in sexual production decreased with increased worker homozygosity. This may either stem from increased homozygosity decreasing the likelihood of diploid brood to develop into queens or a lower efficiency of more homozygous workers at feeding larvae and thus a lower proportion of the female brood developing into queens. There was also a significant negative association between colony age and the level of queen but not worker homozygosity. This association may stem from inbreeding affecting queen lifespan and/or their fecundity, and thus colony survival. However, there was no association between queen homozygosity and colony size, suggesting that inbreeding affects colony survival as a result of inbred queens having a shorter lifespan rather than a lower fecundity. Finally, there was no significant association between either worker or queen homozygosity and the probability of successful colony founding, colony size and colony productivity, the three other traits studied. Overall, these results indicate that inbreeding depression may have important effects on colony fitness by affecting both the parental (queen) and offspring (worker) generations cohabiting within an ant colony.     

Estimation of individual level of inbreeding using relatedness measures in haplodiploids

Although male haploidy in haplodiploid species aids purging of deleterious alleles, haplodiploid animals may nevertheless suffer significant negative effects of inbreeding. The effects may even be stronger in social Hymenoptera because the negative fitness consequences may be expressed at two levels: the individual level (inbred queens) and colony level (inbred workers). Surprisingly, in natural populations the impact of inbreeding on fitness has been studied in very few insects, and even fewer haplodiploid ones. Hence there is currently little understanding of the potential effects of inbreeding. One reason may be the difficulties in estimating inbreeding especially at the individual level, apart from the additional problems posed by haplodiploidy. In order to study the impact of inbreeding, its individual level must be estimated as precisely as possible. When the population pedigree is unknown, relatedness-based estimates of the individual inbreeding coefficient can be used to estimate inbreeding. Here we examine the relationship between inbreeding coefficients and relatedness in diploid and haplodiploid organisms, and provide guidelines for estimating inbreeding both at the individual and the colony level. Received 7 March 2005; revised 18 April 2005, accepted 20 April 2005. An erratum to this article is available at .     

Effects of Increased Flight on the Energetics and Life History of the Butterfly Speyeria mormonia

Movement uses resources that may otherwise be allocated to somatic maintenance or reproduction. How does increased energy expenditure affect resource allocation? Using the butterfly Speyeria mormonia, we tested whether experimentally increased flight affects fecundity, lifespan or flight capacity. We measured body mass (storage), resting metabolic rate and lifespan (repair and maintenance), flight metabolic rate (flight capacity), egg number and composition (reproduction), and food intake across the adult lifespan. The flight treatment did not affect body mass or lifespan. Food intake increased sufficiently to offset the increased energy expenditure. Total egg number did not change, but flown females had higher early-life fecundity and higher egg dry mass than control females. Egg dry mass decreased with age in both treatments. Egg protein, triglyceride or glycogen content did not change with flight or age, but some components tracked egg dry mass. Flight elevated resting metabolic rate, indicating increased maintenance costs. Flight metabolism decreased with age, with a steeper slope for flown females. This may reflect accelerated metabolic senescence from detrimental effects of flight. These effects of a drawdown of nutrients via flight contrast with studies restricting adult nutrient input. There, fecundity was reduced, but flight capacity and lifespan were unchanged. The current study showed that when food resources were abundant, wing-monomorphic butterflies living in a continuous meadow landscape resisted flight-induced stress, exhibiting no evidence of a flight-fecundity or flight-longevity trade-off. Instead, flight changed the dynamics of energy use and reproduction as butterflies adopted a faster lifestyle in early life. High investment in early reproduction may have positive fitness effects in the wild, as long as food is available. Our results help to predict the effect of stressful conditions on the life history of insects living in a changing world.